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Bibliography on: Origin of Eukaryotes

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ESP: PubMed Auto Bibliography 02 Dec 2023 at 01:45 Created: 

Origin of Eukaryotes

The evolutionary origin of eukaryotes is a critically important, yet poorly understood event in the history of life on earth. The endosymbiotic origin of mitochondria allowed cells to become sufficiently large that they could begin to interact mechanically with their surrounding environment, thereby allowing evolution to create the visible biosphere of multicellular eukaryotes.

Created with PubMed® Query: ("origin of eukaryotes"[TIAB] OR eukaryogenesis OR "appearance of eukaryotes"[TIAB] OR "evolution of eukaryotes[TIAB]") NOT pmcbook NOT ispreviousversion

Citations The Papers (from PubMed®)


RevDate: 2023-11-29

Baum B, A Spang (2023)

On the origin of the nucleus: a hypothesis.

Microbiology and molecular biology reviews : MMBR [Epub ahead of print].

SUMMARYIn this hypothesis article, we explore the origin of the eukaryotic nucleus. In doing so, we first look afresh at the nature of this defining feature of the eukaryotic cell and its core functions-emphasizing the utility of seeing the eukaryotic nucleoplasm and cytoplasm as distinct regions of a common compartment. We then discuss recent progress in understanding the evolution of the eukaryotic cell from archaeal and bacterial ancestors, focusing on phylogenetic and experimental data which have revealed that many eukaryotic machines with nuclear activities have archaeal counterparts. In addition, we review the literature describing the cell biology of representatives of the TACK and Asgardarchaeaota - the closest known living archaeal relatives of eukaryotes. Finally, bringing these strands together, we propose a model for the archaeal origin of the nucleus that explains much of the current data, including predictions that can be used to put the model to the test.

RevDate: 2023-11-17

Mahendrarajah TA, Moody ERR, Schrempf D, et al (2023)

ATP synthase evolution on a cross-braced dated tree of life.

Nature communications, 14(1):7456.

The timing of early cellular evolution, from the divergence of Archaea and Bacteria to the origin of eukaryotes, is poorly constrained. The ATP synthase complex is thought to have originated prior to the Last Universal Common Ancestor (LUCA) and analyses of ATP synthase genes, together with ribosomes, have played a key role in inferring and rooting the tree of life. We reconstruct the evolutionary history of ATP synthases using an expanded taxon sampling set and develop a phylogenetic cross-bracing approach, constraining equivalent speciation nodes to be contemporaneous, based on the phylogenetic imprint of endosymbioses and ancient gene duplications. This approach results in a highly resolved, dated species tree and establishes an absolute timeline for ATP synthase evolution. Our analyses show that the divergence of ATP synthase into F- and A/V-type lineages was a very early event in cellular evolution dating back to more than 4 Ga, potentially predating the diversification of Archaea and Bacteria. Our cross-braced, dated tree of life also provides insight into more recent evolutionary transitions including eukaryogenesis, showing that the eukaryotic nuclear and mitochondrial lineages diverged from their closest archaeal (2.67-2.19 Ga) and bacterial (2.58-2.12 Ga) relatives at approximately the same time, with a slightly longer nuclear stem-lineage.

RevDate: 2023-11-08

Garcia PS, Barras F, S Gribaldo (2023)

Components of iron-Sulfur cluster assembly machineries are robust phylogenetic markers to trace the origin of mitochondria and plastids.

PLoS biology, 21(11):e3002374 pii:PBIOLOGY-D-23-00534.

Establishing the origin of mitochondria and plastids is key to understand 2 founding events in the origin and early evolution of eukaryotes. Recent advances in the exploration of microbial diversity and in phylogenomics approaches have indicated a deep origin of mitochondria and plastids during the diversification of Alphaproteobacteria and Cyanobacteria, respectively. Here, we strongly support these placements by analyzing the machineries for assembly of iron-sulfur ([Fe-S]) clusters, an essential function in eukaryotic cells that is carried out in mitochondria by the ISC machinery and in plastids by the SUF machinery. We assessed the taxonomic distribution of ISC and SUF in representatives of major eukaryotic supergroups and analyzed the phylogenetic relationships with their prokaryotic homologues. Concatenation datasets of core ISC proteins show an early branching of mitochondria within Alphaproteobacteria, right after the emergence of Magnetococcales. Similar analyses with the SUF machinery place primary plastids as sister to Gloeomargarita within Cyanobacteria. Our results add to the growing evidence of an early emergence of primary organelles and show that the analysis of essential machineries of endosymbiotic origin provide a robust signal to resolve ancient and fundamental steps in eukaryotic evolution.

RevDate: 2020-11-14
CmpDate: 2020-06-12

Starr DA (2019)

A network of nuclear envelope proteins and cytoskeletal force generators mediates movements of and within nuclei throughout Caenorhabditis elegans development.

Experimental biology and medicine (Maywood, N.J.), 244(15):1323-1332.

UNLABELLED: Nuclear migration and anchorage, together referred to as nuclear positioning, are central to many cellular and developmental events. Nuclear positioning is mediated by a conserved network of nuclear envelope proteins that interacts with force generators in the cytoskeleton. At the heart of this network are linker of nucleoskeleton and cytoskeleton (LINC) complexes made of Sad1 and UNC-84 (SUN) proteins at the inner nuclear membrane and Klarsicht, ANC-1, and Syne homology (KASH) proteins in the outer nuclear membrane. LINC complexes span the nuclear envelope, maintain nuclear envelope architecture, designate the surface of nuclei distinctly from the contiguous endoplasmic reticulum, and were instrumental in the early evolution of eukaryotes. LINC complexes interact with lamins in the nucleus and with various cytoplasmic KASH effectors from the surface of nuclei. These effectors regulate the cytoskeleton, leading to a variety of cellular outputs including pronuclear migration, nuclear migration through constricted spaces, nuclear anchorage, centrosome attachment to nuclei, meiotic chromosome movements, and DNA damage repair. How LINC complexes are regulated and how they function are reviewed here. The focus is on recent studies elucidating the best-understood network of LINC complexes, those used throughout Caenorhabditis elegans development.

IMPACT STATEMENT: Defects in nuclear positioning disrupt development in many mammalian tissues. In human development, LINC complexes play important cellular functions including nuclear positioning, homolog pairing in meiosis, DNA damage repair, wound healing, and gonadogenesis. The topics reviewed here are relevant to public health because defects in nuclear positioning and mutations in LINC components are associated with a wide variety of human diseases including muscular dystrophies, neurological disorders, progeria, aneurysms, hearing loss, blindness, sterility, and multiple cancers. Although this review focuses on findings in the model nematode Caenorhabditis elegans, the studies are relevant because almost all the findings originally made in C. elegans are conserved to humans. Furthermore, C. elegans remains the best described network for how LINC complexes are regulated and function.

RevDate: 2023-10-16

Câmara AS, Kubalová I, V Schubert (2023)

Helical chromonema coiling is conserved in eukaryotes.

The Plant journal : for cell and molecular biology [Epub ahead of print].

Efficient chromatin condensation is required to transport chromosomes during mitosis and meiosis, forming daughter cells. While it is well accepted that these processes follow fundamental rules, there has been a controversial debate for more than 140 years on whether the higher-order chromatin organization in chromosomes is evolutionarily conserved. Here, we summarize historical and recent investigations based on classical and modern methods. In particular, classical light microscopy observations based on living, fixed, and treated chromosomes covering a wide range of plant and animal species, and even in single-cell eukaryotes suggest that the chromatids of large chromosomes are formed by a coiled chromatin thread, named the chromonema. More recently, these findings were confirmed by electron and super-resolution microscopy, oligo-FISH, molecular interaction data, and polymer simulation. Altogether, we describe common and divergent features of coiled chromonemata in different species. We hypothesize that chromonema coiling in large chromosomes is a fundamental feature established early during the evolution of eukaryotes to handle increasing genome sizes.

RevDate: 2023-10-07

Weston EJ, Eglit Y, AGB Simpson (2023)

Kaonashia insperata gen. et sp. nov., a eukaryotrophic flagellate, represents a novel major lineage of heterotrophic stramenopiles.

The Journal of eukaryotic microbiology [Epub ahead of print].

Eukaryotrophic protists are ecologically significant and possess characteristics key to understanding the evolution of eukaryotes; however, they remain poorly studied, due partly to the complexities of maintaining predator-prey cultures. Kaonashia insperata, gen. nov., et sp. nov., is a free-swimming biflagellated eukaryotroph with a conspicuous ventral groove, a trait observed in distantly related lineages across eukaryote diversity. Di-eukaryotic (predator-prey) cultures of K. insperata with three marine algae (Isochrysis galbana, Guillardia theta, and Phaeodactylum tricornutum) were established by single-cell isolation. Growth trials showed that the studied K. insperata clone grew particularly well on G. theta, reaching a peak abundance of 1.0 × 10[5] ± 4.0 × 10[4] cells ml[-1] . Small-subunit ribosomal DNA phylogenies infer that K. insperata is a stramenopile with moderate support; however, it does not fall within any well-defined phylogenetic group, including environmental sequence clades (e.g. MASTs), and its specific placement remains unresolved. Electron microscopy shows traits consistent with stramenopile affinity, including mastigonemes on the anterior flagellum and tubular mitochondrial cristae. Kaonashia insperata may represent a novel major lineage within stramenopiles, and be important for understanding the evolutionary history of the group. While heterotrophic stramenopile flagellates are considered to be predominantly bacterivorous, eukaryotrophy may be relatively widespread amongst this assemblage.

RevDate: 2023-10-03

Wegner L, Porth ML, K Ehlers (2023)

Multicellularity and the Need for Communication-A Systematic Overview on (Algal) Plasmodesmata and Other Types of Symplasmic Cell Connections.

Plants (Basel, Switzerland), 12(18):.

In the evolution of eukaryotes, the transition from unicellular to simple multicellular organisms has happened multiple times. For the development of complex multicellularity, characterized by sophisticated body plans and division of labor between specialized cells, symplasmic intercellular communication is supposed to be indispensable. We review the diversity of symplasmic connectivity among the eukaryotes and distinguish between distinct types of non-plasmodesmatal connections, plasmodesmata-like structures, and 'canonical' plasmodesmata on the basis of developmental, structural, and functional criteria. Focusing on the occurrence of plasmodesmata (-like) structures in extant taxa of fungi, brown algae (Phaeophyceae), green algae (Chlorophyta), and streptophyte algae, we present a detailed critical update on the available literature which is adapted to the present classification of these taxa and may serve as a tool for future work. From the data, we conclude that, actually, development of complex multicellularity correlates with symplasmic connectivity in many algal taxa, but there might be alternative routes. Furthermore, we deduce a four-step process towards the evolution of canonical plasmodesmata and demonstrate similarity of plasmodesmata in streptophyte algae and land plants with respect to the occurrence of an ER component. Finally, we discuss the urgent need for functional investigations and molecular work on cell connections in algal organisms.

RevDate: 2023-09-21

Craig JM, Kumar S, SB Hedges (2023)

The origin of eukaryotes and rise in complexity were synchronous with the rise in oxygen.

Frontiers in bioinformatics, 3:1233281.

The origin of eukaryotes was among the most important events in the history of life, spawning a new evolutionary lineage that led to all complex multicellular organisms. However, the timing of this event, crucial for understanding its environmental context, has been difficult to establish. The fossil and biomarker records are sparse and molecular clocks have thus far not reached a consensus, with dates spanning 2.1-0.91 billion years ago (Ga) for critical nodes. Notably, molecular time estimates for the last common ancestor of eukaryotes are typically hundreds of millions of years younger than the Great Oxidation Event (GOE, 2.43-2.22 Ga), leading researchers to question the presumptive link between eukaryotes and oxygen. We obtained a new time estimate for the origin of eukaryotes using genetic data of both archaeal and bacterial origin, the latter rarely used in past studies. We also avoided potential calibration biases that may have affected earlier studies. We obtained a conservative interval of 2.2-1.5 Ga, with an even narrower core interval of 2.0-1.8 Ga, for the origin of eukaryotes, a period closely aligned with the rise in oxygen. We further reconstructed the history of biological complexity across the tree of life using three universal measures: cell types, genes, and genome size. We found that the rise in complexity was temporally consistent with and followed a pattern similar to the rise in oxygen. This suggests a causal relationship stemming from the increased energy needs of complex life fulfilled by oxygen.

RevDate: 2023-09-20
CmpDate: 2023-09-18

Porter SM, LA Riedman (2023)

Frameworks for Interpreting the Early Fossil Record of Eukaryotes.

Annual review of microbiology, 77:173-191.

The origin of modern eukaryotes is one of the key transitions in life's history, and also one of the least understood. Although the fossil record provides the most direct view of this process, interpreting the fossils of early eukaryotes and eukaryote-grade organisms is not straightforward. We present two end-member models for the evolution of modern (i.e., crown) eukaryotes-one in which modern eukaryotes evolved early, and another in which they evolved late-and interpret key fossils within these frameworks, including where they might fit in eukaryote phylogeny and what they may tell us about the evolution of eukaryotic cell biology and ecology. Each model has different implications for understanding the rise of complex life on Earth, including different roles of Earth surface oxygenation, and makes different predictions that future paleontological studies can test.

RevDate: 2023-09-21
CmpDate: 2023-09-14

Donoghue PCJ, Kay C, Spang A, et al (2023)

Defining eukaryotes to dissect eukaryogenesis.

Current biology : CB, 33(17):R919-R929.

The origin of eukaryotes is among the most contentious debates in evolutionary biology, attracting multiple seemingly incompatible theories seeking to explain the sequence in which eukaryotic characteristics were acquired. Much of the controversy arises from differing views on the defining characteristics of eukaryotes. We argue that eukaryotes should be defined phylogenetically, and that doing so clarifies where competing hypotheses of eukaryogenesis agree and how we may test among aspects of disagreement. Some hypotheses make predictions about the phylogenetic origins of eukaryotic genes and are distinguishable on that basis. However, other hypotheses differ only in the order of key evolutionary steps, like mitochondrial endosymbiosis and nuclear assembly, which cannot currently be distinguished phylogenetically. Stages within eukaryogenesis may be made identifiable through the absolute dating of gene duplicates that map to eukaryotic traits, such as in genes of host or mitochondrial origin that duplicated and diverged functionally prior to emergence of the last eukaryotic common ancestor. In this way, it may finally be possible to distinguish heat from light in the debate over eukaryogenesis.

RevDate: 2023-09-04

Field MC (2023)

Deviating from the norm: Nuclear organisation in trypanosomes.

Current opinion in cell biology, 85:102234 pii:S0955-0674(23)00083-2 [Epub ahead of print].

At first glance the nucleus is a highly conserved organelle. Overall nuclear morphology, the octagonal nuclear pore complex, the presence of peripheral heterochromatin and the nuclear envelope appear near constant features right down to the ultrastructural level. New work is revealing significant compositional divergence within these nuclear structures and their associated functions, likely reflecting adaptations and distinct mechanisms between eukaryotic lineages and especially the trypanosomatids. While many examples of mechanistic divergence currently lack obvious functional interpretations, these studies underscore the malleability of nuclear architecture. I will discuss some recent findings highlighting these facets within trypanosomes, together with the underlying evolutionary framework and make a call for the exploration of nuclear function in non-canonical experimental organisms.

RevDate: 2023-09-07
CmpDate: 2023-08-28

Gaïa M, P Forterre (2023)

From Mimivirus to Mirusvirus: The Quest for Hidden Giants.

Viruses, 15(8):.

Our perception of viruses has been drastically evolving since the inception of the field of virology over a century ago. In particular, the discovery of giant viruses from the Nucleocytoviricota phylum marked a pivotal moment. Their previously concealed diversity and abundance unearthed an unprecedented complexity in the virus world, a complexity that called for new definitions and concepts. These giant viruses underscore the intricate interactions that unfold over time between viruses and their hosts, and are themselves suspected to have played a significant role as a driving force in the evolution of eukaryotes since the dawn of this cellular domain. Whether they possess exceptional relationships with their hosts or whether they unveil the actual depths of evolutionary connections between viruses and cells otherwise hidden in smaller viruses, the attraction giant viruses exert on the scientific community and beyond continues to grow. Yet, they still hold surprises. Indeed, the recent identification of mirusviruses connects giant viruses to herpesviruses, each belonging to distinct viral realms. This discovery substantially broadens the evolutionary landscape of Nucleocytoviricota. Undoubtedly, the years to come will reveal their share of surprises.

RevDate: 2023-08-22

Yubuki N, Torruella G, Galindo LJ, et al (2023)

Molecular and morphological characterization of four new ancyromonad genera and proposal for an updated taxonomy of the Ancyromonadida.

The Journal of eukaryotic microbiology [Epub ahead of print].

Ancyromonads are small biflagellated protists with a bean-shaped morphology. They are cosmopolitan in marine, freshwater, and soil environments, where they attach to surfaces while feeding on bacteria. These poorly known grazers stand out by their uncertain phylogenetic position in the tree of eukaryotes, forming a deep-branching "orphan" lineage that is considered key to a better understanding of the early evolution of eukaryotes. Despite their ecological and evolutionary interest, only limited knowledge exists about their true diversity. Here, we aimed to characterize ancyromonads better by integrating environmental surveys with behavioral observation and description of cell morphology, for which sample isolation and culturing are indispensable. We studied 18 ancyromonad strains, including 14 new isolates and seven new species. We described three new and genetically divergent genera: Caraotamonas, Nyramonas, and Olneymonas, together encompassing four species. The remaining three new species belong to the already-known genera Fabomonas and Ancyromonas. We also raised Striomonas, formerly a subgenus of Nutomonas, to full genus status, on morphological and phylogenetic grounds. We studied the morphology of diverse ancyromonads under light and electron microscopy and carried out molecular phylogenetic analyses, also including 18S rRNA gene sequences from several environmental surveys. Based on these analyses, we have updated the taxonomy of Ancyromonadida.

RevDate: 2023-10-03
CmpDate: 2023-09-18

van Hooff JJE (2023)

Towards unraveling the origins of eukaryotic nuclear genome organization.

Trends in cell biology, 33(10):820-823.

With 3D genome mapping maturing over the past decade, studies exposed the differences between eukaryotic and prokaryotic genome organization. This raises the question of how the complex eukaryotic genome organization originated. Here, I explore potential pathways to answering this question, guided by our changing understanding of the origins of eukaryotes.

RevDate: 2023-08-08

Hernández G, P Vazquez-Pianzola (2023)

eIF4E as a molecular wildcard in metazoans RNA metabolism.

Biological reviews of the Cambridge Philosophical Society [Epub ahead of print].

The evolutionary origin of eukaryotes spurred the transition from prokaryotic-like translation to a more sophisticated, eukaryotic translation. During this process, successive gene duplication of a single, primordial eIF4E gene encoding the mRNA cap-binding protein eukaryotic translation initiation factor 4E (eIF4E) gave rise to a plethora of paralog genes across eukaryotes that underwent further functional diversification in RNA metabolism. The ability to take different roles is due to eIF4E promiscuity in binding many partner proteins, rendering eIF4E a highly versatile and multifunctional player that functions as a molecular wildcard. Thus, in metazoans, eIF4E paralogs are involved in various processes, including messenger RNA (mRNA) processing, export, translation, storage, and decay. Moreover, some paralogs display differential expression in tissues and developmental stages and show variable biochemical properties. In this review, we discuss recent advances shedding light on the functional diversification of eIF4E in metazoans. We emphasise humans and two phylogenetically distant species which have become paradigms for studies on development, namely the fruit fly Drosophila melanogaster and the roundworm Caenorhabditis elegans.

RevDate: 2023-08-01
CmpDate: 2023-07-31

Kordiš D, V Turk (2023)

Origin and Early Diversification of the Papain Family of Cysteine Peptidases.

International journal of molecular sciences, 24(14):.

Peptidases of the papain family play a key role in protein degradation, regulated proteolysis, and the host-pathogen arms race. Although the papain family has been the subject of many studies, knowledge about its diversity, origin, and evolution in Eukaryota, Bacteria, and Archaea is limited; thus, we aimed to address these long-standing knowledge gaps. We traced the origin and expansion of the papain family with a phylogenomic analysis, using sequence data from numerous prokaryotic and eukaryotic proteomes, transcriptomes, and genomes. We identified the full complement of the papain family in all prokaryotic and eukaryotic lineages. Analysis of the papain family provided strong evidence for its early diversification in the ancestor of eukaryotes. We found that the papain family has undergone complex and dynamic evolution through numerous gene duplications, which produced eight eukaryotic ancestral paralogous C1A lineages during eukaryogenesis. Different evolutionary forces operated on C1A peptidases, including gene duplication, horizontal gene transfer, and gene loss. This study challenges the current understanding of the origin and evolution of the papain family and provides valuable insights into their early diversification. The findings of this comprehensive study provide guidelines for future structural and functional studies of the papain family.

RevDate: 2023-10-09

Esposti MD (2023)

Eukaryotes inherited inositol lipids from bacteria: implications for the models of eukaryogenesis.

FEBS letters, 597(19):2484-2496.

The merger of two very different microbes, an anaerobic archaeon and an aerobic bacterium, led to the birth of eukaryotic cells. Current models hypothesize that an archaeon engulfed bacteria through external protrusions that then fused together forming the membrane organelles of eukaryotic cells, including mitochondria. Images of cultivated Lokiarchaea sustain this concept, first proposed in the inside-out model which assumes that the membrane traffic system of archaea drove the merging with bacterial cells through membrane expansions containing inositol lipids, considered to have evolved first in archaea. This assumption has been evaluated here in detail. The data indicate that inositol lipids first emerged in bacteria, not in archaea. The implications of this finding for the models of eukaryogenesis are discussed.

RevDate: 2023-07-29
CmpDate: 2023-07-27

von der Dunk SHA, Hogeweg P, B Snel (2023)

Obligate endosymbiosis enables genome expansion during eukaryogenesis.

Communications biology, 6(1):777.

The endosymbiosis of an alpha-proteobacterium that gave rise to mitochondria was one of the key events in eukaryogenesis. One striking outcome of eukaryogenesis was a much more complex cell with a large genome. Despite the existence of many alternative hypotheses for this and other patterns potentially related to endosymbiosis, a constructive evolutionary model in which these hypotheses can be studied is still lacking. Here, we present a theoretical approach in which we focus on the consequences rather than the causes of mitochondrial endosymbiosis. Using a constructive evolutionary model of cell-cycle regulation, we find that genome expansion and genome size asymmetry arise from emergent host-symbiont cell-cycle coordination. We also find that holobionts with large host and small symbiont genomes perform best on long timescales and mimic the outcome of eukaryogenesis. By designing and studying a constructive evolutionary model of obligate endosymbiosis, we uncovered some of the forces that may drive the patterns observed in nature. Our results provide a theoretical foundation for patterns related to mitochondrial endosymbiosis, such as genome size asymmetry, and reveal evolutionary outcomes that have not been considered so far, such as cell-cycle coordination without direct communication.

RevDate: 2023-08-14
CmpDate: 2023-08-14

Gollo G (2023)

On the emergence of eukaryotes and other enigmas.

Bio Systems, 231:104958.

The origin of eukaryotes is one of the most fundamental problems in the entire history of life. How did eukaryotes arise? Previous attempts to solve the problem are very far from an answer, at best they propose a solution to one of the various innovations that ended up culminating in eukaryotes. Based on a hypothetical-deductive methodology, as usual in evolutionary issues, I propose that eukaryotes emerged from the endosymbiotic association between a flagellate parasite and its host, of which the sperm is the main vestige. The hypothesis unifies the solution to the vast array of acquisitions shared by eukaryotes that differentiate them from other beings, remarkably cell nucleus, mitosis, meiosis and sexual reproduction. The solution has a deep impact on understanding the origin and functioning of all complex life forms.

RevDate: 2023-07-05
CmpDate: 2023-07-05

Eme L, Tamarit D, Caceres EF, et al (2023)

Inference and reconstruction of the heimdallarchaeial ancestry of eukaryotes.

Nature, 618(7967):992-999.

In the ongoing debates about eukaryogenesis-the series of evolutionary events leading to the emergence of the eukaryotic cell from prokaryotic ancestors-members of the Asgard archaea play a key part as the closest archaeal relatives of eukaryotes[1]. However, the nature and phylogenetic identity of the last common ancestor of Asgard archaea and eukaryotes remain unresolved[2-4]. Here we analyse distinct phylogenetic marker datasets of an expanded genomic sampling of Asgard archaea and evaluate competing evolutionary scenarios using state-of-the-art phylogenomic approaches. We find that eukaryotes are placed, with high confidence, as a well-nested clade within Asgard archaea and as a sister lineage to Hodarchaeales, a newly proposed order within Heimdallarchaeia. Using sophisticated gene tree and species tree reconciliation approaches, we show that analogous to the evolution of eukaryotic genomes, genome evolution in Asgard archaea involved significantly more gene duplication and fewer gene loss events compared with other archaea. Finally, we infer that the last common ancestor of Asgard archaea was probably a thermophilic chemolithotroph and that the lineage from which eukaryotes evolved adapted to mesophilic conditions and acquired the genetic potential to support a heterotrophic lifestyle. Our work provides key insights into the prokaryote-to-eukaryote transition and a platform for better understanding the emergence of cellular complexity in eukaryotic cells.

RevDate: 2023-06-16
CmpDate: 2023-06-07

Kumar P, Babu KSD, Singh AK, et al (2023)

Distinct localization of chiral proofreaders resolves organellar translation conflict in plants.

Proceedings of the National Academy of Sciences of the United States of America, 120(24):e2219292120.

Plants have two endosymbiotic organelles originated from two bacterial ancestors. The transition from an independent bacterium to a successful organelle would have required extensive rewiring of biochemical networks for its integration with archaeal host. Here, using Arabidopsis as a model system, we show that plant D-aminoacyl-tRNA deacylase 1 (DTD1), of bacterial origin, is detrimental to organellar protein synthesis owing to its changed tRNA recognition code. Plants survive this conflict by spatially restricting the conflicted DTD1 to the cytosol. In addition, plants have targeted archaeal DTD2 to both the organelles as it is compatible with their translation machinery due to its strict D-chiral specificity and lack of tRNA determinants. Intriguingly, plants have confined bacterial-derived DTD1 to work in archaeal-derived cytosolic compartment whereas archaeal DTD2 is targeted to bacterial-derived organelles. Overall, the study provides a remarkable example of the criticality of optimization of biochemical networks for survival and evolution of plant mitochondria and chloroplast.

RevDate: 2023-10-02
CmpDate: 2023-06-01

López-García P, D Moreira (2023)

The symbiotic origin of the eukaryotic cell.

Comptes rendus biologies, 346:55-73.

Eukaryogenesis represented a major evolutionary transition that led to the emergence of complex cells from simpler ancestors. For several decades, the most accepted scenario involved the evolution of an independent lineage of proto-eukaryotes endowed with an endomembrane system, including a nuclear compartment, a developed cytoskeleton and phagocytosis, which engulfed the alphaproteobacterial ancestor of mitochondria. However, the recent discovery by metagenomic and cultural approaches of Asgard archaea, which harbour many genes in common with eukaryotes and are their closest relatives in phylogenomic trees, rather supports scenarios based on the symbiosis of one Asgard-like archaeon and one or more bacteria at the origin of the eukaryotic cell. Here, we review the recent discoveries that led to this conceptual shift, briefly evoking current models of eukaryogenesis and the challenges ahead to discriminate between them and to establish a detailed, plausible scenario that accounts for the evolution of eukaryotic traits from those of their prokaryotic ancestors.

RevDate: 2023-09-15
CmpDate: 2023-08-25

Řezanka T, Kyselová L, DJ Murphy (2023)

Archaeal lipids.

Progress in lipid research, 91:101237.

The major archaeal membrane glycerolipids are distinguished from those of bacteria and eukaryotes by the contrasting stereochemistry of their glycerol backbones, and by the use of ether-linked isoprenoid-based alkyl chains rather than ester-linked fatty acyl chains for their hydrophobic moieties. These fascinating compounds play important roles in the extremophile lifestyles of many species, but are also present in the growing numbers of recently discovered mesophilic archaea. The past decade has witnessed significant advances in our understanding of archaea in general and their lipids in particular. Much of the new information has come from the ability to screen large microbial populations via environmental metagenomics, which has revolutionised our understanding of the extent of archaeal biodiversity that is coupled with a strict conservation of their membrane lipid compositions. Significant additional progress has come from new culturing and analytical techniques that are gradually enabling archaeal physiology and biochemistry to be studied in real time. These studies are beginning to shed light on the much-discussed and still-controversial process of eukaryogenesis, which probably involved both bacterial and archaeal progenitors. Puzzlingly, although eukaryotes retain many attributes of their putative archaeal ancestors, their lipid compositions only reflect their bacterial progenitors. Finally, elucidation of archaeal lipids and their metabolic pathways have revealed potentially interesting applications that have opened up new frontiers for biotechnological exploitation of these organisms. This review is concerned with the analysis, structure, function, evolution and biotechnology of archaeal lipids and their associated metabolic pathways.

RevDate: 2023-06-12
CmpDate: 2023-06-05

Krupovic M, Dolja VV, EV Koonin (2023)

The virome of the last eukaryotic common ancestor and eukaryogenesis.

Nature microbiology, 8(6):1008-1017.

All extant eukaryotes descend from the last eukaryotic common ancestor (LECA), which is thought to have featured complex cellular organization. To gain insight into LECA biology and eukaryogenesis-the origin of the eukaryotic cell, which remains poorly understood-we reconstructed the LECA virus repertoire. We compiled an inventory of eukaryotic hosts of all major virus taxa and reconstructed the LECA virome by inferring the origins of these groups of viruses. The origin of the LECA virome can be traced back to a small set of bacterial-not archaeal-viruses. This provenance of the LECA virome is probably due to the bacterial origin of eukaryotic membranes, which is most compatible with two endosymbiosis events in a syntrophic model of eukaryogenesis. In the first endosymbiosis, a bacterial host engulfed an Asgard archaeon, preventing archaeal viruses from entry owing to a lack of archaeal virus receptors on the external membranes.

RevDate: 2023-05-25
CmpDate: 2023-05-25

Su H, Xu J, Li J, et al (2023)

Four ciliate-specific expansion events occurred during actin gene family evolution of eukaryotes.

Molecular phylogenetics and evolution, 184:107789.

Actin gene family is a divergent and ancient eukaryotic cellular cytoskeletal gene family, and participates in many essential cellular processes. Ciliated protists offer us an excellent opportunity to investigate gene family evolution, since their gene families evolved faster in ciliates than in other eukaryotes. Nonetheless, actin gene family is well studied in few model ciliate species but little is known about its evolutionary patterns in ciliates. Here, we analyzed the evolutionary pattern of eukaryotic actin gene family based on genomes/transcriptomes of 36 species covering ten ciliate classes, as well as those of nine non-ciliate eukaryotic species. Results showed: (1) Except for conventional actins and actin-related proteins (Arps) shared by various eukaryotes, at least four ciliate-specific subfamilies occurred during evolution of actin gene family. Expansions of Act2 and ArpC were supposed to have happened in the ciliate common ancestor, while expansions of ActI and ActII may have occurred in the ancestor of Armophorea, Muranotrichea, and Spirotrichea. (2) The number of actin isoforms varied greatly among ciliate species. Environmental adaptability, whole genome duplication (WGD) or segmental duplication events, distinct spatial and temporal patterns of expression might play driving forces for the variation of isoform numbers. (3) The 'birth and death' model of evolution could explain the evolution of actin gene family in ciliates. And actin genes have been generally under strong negative selection to maintain protein structures and physiological functions. Collectively, we provided meaningful information for understanding the evolution of eukaryotic actin gene family.

RevDate: 2023-05-09
CmpDate: 2023-04-20

Libby E, Kempes CP, JG Okie (2023)

Metabolic compatibility and the rarity of prokaryote endosymbioses.

Proceedings of the National Academy of Sciences of the United States of America, 120(17):e2206527120.

The evolution of the mitochondria was a significant event that gave rise to the eukaryotic lineage and most large complex life. Central to the origins of the mitochondria was an endosymbiosis between prokaryotes. Yet, despite the potential benefits that can stem from a prokaryotic endosymbiosis, their modern occurrence is exceptionally rare. While many factors may contribute to their rarity, we lack methods for estimating the extent to which they constrain the appearance of a prokaryotic endosymbiosis. Here, we address this knowledge gap by examining the role of metabolic compatibility between a prokaryotic host and endosymbiont. We use genome-scale metabolic flux models from three different collections (AGORA, KBase, and CarveMe) to assess the viability, fitness, and evolvability of potential prokaryotic endosymbioses. We find that while more than half of host-endosymbiont pairings are metabolically viable, the resulting endosymbioses have reduced growth rates compared to their ancestral metabolisms and are unlikely to gain mutations to overcome these fitness differences. In spite of these challenges, we do find that they may be more robust in the face of environmental perturbations at least in comparison with the ancestral host metabolism lineages. Our results provide a critical set of null models and expectations for understanding the forces that shape the structure of prokaryotic life.

RevDate: 2023-05-25
CmpDate: 2023-05-17

Speijer D (2023)

How mitochondria showcase evolutionary mechanisms and the importance of oxygen.

BioEssays : news and reviews in molecular, cellular and developmental biology, 45(6):e2300013.

Darwinian evolution can be simply stated: natural selection of inherited variations increasing differential reproduction. However, formulated thus, links with biochemistry, cell biology, ecology, and population dynamics remain unclear. To understand interactive contributions of chance and selection, higher levels of biological organization (e.g., endosymbiosis), complexities of competing selection forces, and emerging biological novelties (such as eukaryotes or meiotic sex), we must analyze actual examples. Focusing on mitochondria, I will illuminate how biology makes sense of life's evolution, and the concepts involved. First, looking at the bacterium - mitochondrion transition: merging with an archaeon, it lost its independence, but played a decisive role in eukaryogenesis, as an extremely efficient aerobic ATP generator and internal ROS source. Second, surveying later mitochondrion adaptations and diversifications illustrates concepts such as constructive neutral evolution, dynamic interactions between endosymbionts and hosts, the contingency of life histories, and metabolic reprogramming. Without oxygen, mitochondria disappear; with (intermittent) oxygen diversification occurs in highly complex ways, especially upon (temporary) phototrophic substrate supply. These expositions show the Darwinian model to be a highly fruitful paradigm.

RevDate: 2023-04-15
CmpDate: 2023-03-30

Muñoz-Gómez SA, Cadena LR, Gardiner AT, et al (2023)

Intracytoplasmic-membrane development in alphaproteobacteria involves the homolog of the mitochondrial crista-developing protein Mic60.

Current biology : CB, 33(6):1099-1111.e6.

Mitochondrial cristae expand the surface area of respiratory membranes and ultimately allow for the evolutionary scaling of respiration with cell volume across eukaryotes. The discovery of Mic60 homologs among alphaproteobacteria, the closest extant relatives of mitochondria, suggested that cristae might have evolved from bacterial intracytoplasmic membranes (ICMs). Here, we investigated the predicted structure and function of alphaproteobacterial Mic60, and a protein encoded by an adjacent gene Orf52, in two distantly related purple alphaproteobacteria, Rhodobacter sphaeroides and Rhodopseudomonas palustris. In addition, we assessed the potential physical interactors of Mic60 and Orf52 in R. sphaeroides. We show that the three α helices of mitochondrial Mic60's mitofilin domain, as well as its adjacent membrane-binding amphipathic helix, are present in alphaproteobacterial Mic60. The disruption of Mic60 and Orf52 caused photoheterotrophic growth defects, which are most severe under low light conditions, and both their disruption and overexpression led to enlarged ICMs in both studied alphaproteobacteria. We also found that alphaproteobacterial Mic60 physically interacts with BamA, the homolog of Sam50, one of the main physical interactors of eukaryotic Mic60. This interaction, responsible for making contact sites at mitochondrial envelopes, has been conserved in modern alphaproteobacteria despite more than a billion years of evolutionary divergence. Our results suggest a role for Mic60 in photosynthetic ICM development and contact site formation at alphaproteobacterial envelopes. Overall, we provide support for the hypothesis that mitochondrial cristae evolved from alphaproteobacterial ICMs and have therefore improved our understanding of the nature of the mitochondrial ancestor.

RevDate: 2023-03-10
CmpDate: 2023-02-17

Filée J, Becker HF, Mellottee L, et al (2023)

Bacterial origins of thymidylate metabolism in Asgard archaea and Eukarya.

Nature communications, 14(1):838.

Asgard archaea include the closest known archaeal relatives of eukaryotes. Here, we investigate the evolution and function of Asgard thymidylate synthases and other folate-dependent enzymes required for the biosynthesis of DNA, RNA, amino acids and vitamins, as well as syntrophic amino acid utilization. Phylogenies of Asgard folate-dependent enzymes are consistent with their horizontal transmission from various bacterial groups. We experimentally validate the functionality of thymidylate synthase ThyX of the cultured 'Candidatus Prometheoarchaeum syntrophicum'. The enzyme efficiently uses bacterial-like folates and is inhibited by mycobacterial ThyX inhibitors, even though the majority of experimentally tested archaea are known to use carbon carriers distinct from bacterial folates. Our phylogenetic analyses suggest that the eukaryotic thymidylate synthase, required for de novo DNA synthesis, is not closely related to archaeal enzymes and might have been transferred from bacteria to protoeukaryotes during eukaryogenesis. Altogether, our study suggests that the capacity of eukaryotic cells to duplicate their genetic material is a sum of archaeal (replisome) and bacterial (thymidylate synthase) characteristics. We also propose that recent prevalent lateral gene transfer from bacteria has markedly shaped the metabolism of Asgard archaea.

RevDate: 2023-06-10
CmpDate: 2023-03-07

Bremer N, Tria FDK, Skejo J, et al (2023)

The Ancestral Mitotic State: Closed Orthomitosis With Intranuclear Spindles in the Syncytial Last Eukaryotic Common Ancestor.

Genome biology and evolution, 15(3):.

All eukaryotes have linear chromosomes that are distributed to daughter nuclei during mitotic division, but the ancestral state of nuclear division in the last eukaryotic common ancestor (LECA) is so far unresolved. To address this issue, we have employed ancestral state reconstructions for mitotic states that can be found across the eukaryotic tree concerning the intactness of the nuclear envelope during mitosis (open or closed), the position of spindles (intranuclear or extranuclear), and the symmetry of spindles being either axial (orthomitosis) or bilateral (pleuromitosis). The data indicate that the LECA possessed closed orthomitosis with intranuclear spindles. Our reconstruction is compatible with recent findings indicating a syncytial state of the LECA, because it decouples three main processes: chromosome division, chromosome partitioning, and cell division (cytokinesis). The possession of closed mitosis using intranuclear spindles adds to the number of cellular traits that can now be attributed to LECA, providing insights into the lifestyle of this otherwise elusive biological entity at the origin of eukaryotic cells. Closed mitosis in a syncytial eukaryotic common ancestor would buffer mutations arising at the origin of mitotic division by allowing nuclei with viable chromosome sets to complement defective nuclei via mRNA in the cytosol.

RevDate: 2023-02-01
CmpDate: 2023-01-26

Forterre P, M Gaïa (2022)

[Viruses and the evolution of modern eukaryotic cells].

Medecine sciences : M/S, 38(12):990-998.

It is now well accepted that viruses have played an important role in the evolution of modern eukaryotes. In this review, we suggest that interactions between ancient eukaryoviruses and proto-eukaryotes also played a major role in eukaryogenesis. We discuss phylogenetic analyses that highlight the viral origin of several key proteins in the molecular biology of eukaryotes. We also discuss recent observations that, by analogy, could suggest a viral origin of the cellular nucleus. Finally, we hypothesize that mechanisms of cell differentiation in multicellular organisms might have originated from mechanisms implemented by viruses to transform infected cells into virocells.

RevDate: 2023-02-02
CmpDate: 2023-01-24

Santos FB, LE Del-Bem (2022)

The Evolution of tRNA Copy Number and Repertoire in Cellular Life.

Genes, 14(1):.

tRNAs are universal decoders that bridge the gap between transcriptome and proteome. They can also be processed into small RNA fragments with regulatory functions. In this work, we show that tRNA copy number is largely controlled by genome size in all cellular organisms, in contrast to what is observed for protein-coding genes that stop expanding between ~20,000 and ~35,000 loci per haploid genome in eukaryotes, regardless of genome size. Our analyses indicate that after the bacteria/archaea split, the tRNA gene pool experienced the evolution of increased anticodon diversity in the archaeal lineage, along with a tRNA gene size increase and mature tRNA size decrease. The evolution and diversification of eukaryotes from archaeal ancestors involved further expansion of the tRNA anticodon repertoire, additional increase in tRNA gene size and decrease in mature tRNA length, along with an explosion of the tRNA gene copy number that emerged coupled with accelerated genome size expansion. Our findings support the notion that macroscopic eukaryotes with a high diversity of cell types, such as land plants and vertebrates, independently evolved a high diversity of tRNA anticodons along with high gene redundancy caused by the expansion of the tRNA copy number. The results presented here suggest that the evolution of tRNA genes played important roles in the early split between bacteria and archaea, and in eukaryogenesis and the later emergence of complex eukaryotes, with potential implications in protein translation and gene regulation through tRNA-derived RNA fragments.

RevDate: 2023-02-14
CmpDate: 2023-02-01

Vosseberg J, Stolker D, von der Dunk SHA, et al (2023)

Integrating Phylogenetics With Intron Positions Illuminates the Origin of the Complex Spliceosome.

Molecular biology and evolution, 40(1):.

Eukaryotic genes are characterized by the presence of introns that are removed from pre-mRNA by a spliceosome. This ribonucleoprotein complex is comprised of multiple RNA molecules and over a hundred proteins, which makes it one of the most complex molecular machines that originated during the prokaryote-to-eukaryote transition. Previous works have established that these introns and the spliceosomal core originated from self-splicing introns in prokaryotes. Yet, how the spliceosomal core expanded by recruiting many additional proteins remains largely elusive. In this study, we use phylogenetic analyses to infer the evolutionary history of 145 proteins that we could trace back to the spliceosome in the last eukaryotic common ancestor. We found that an overabundance of proteins derived from ribosome-related processes was added to the prokaryote-derived core. Extensive duplications of these proteins substantially increased the complexity of the emerging spliceosome. By comparing the intron positions between spliceosomal paralogs, we infer that most spliceosomal complexity postdates the spread of introns through the proto-eukaryotic genome. The reconstruction of early spliceosomal evolution provides insight into the driving forces behind the emergence of complexes with many proteins during eukaryogenesis.

RevDate: 2023-06-10
CmpDate: 2023-01-31

Otsuka S, Tempkin JOB, Zhang W, et al (2023)

A quantitative map of nuclear pore assembly reveals two distinct mechanisms.

Nature, 613(7944):575-581.

Understanding how the nuclear pore complex (NPC) is assembled is of fundamental importance to grasp the mechanisms behind its essential function and understand its role during the evolution of eukaryotes[1-4]. There are at least two NPC assembly pathways-one during the exit from mitosis and one during nuclear growth in interphase-but we currently lack a quantitative map of these events. Here we use fluorescence correlation spectroscopy calibrated live imaging of endogenously fluorescently tagged nucleoporins to map the changes in the composition and stoichiometry of seven major modules of the human NPC during its assembly in single dividing cells. This systematic quantitative map reveals that the two assembly pathways have distinct molecular mechanisms, in which the order of addition of two large structural components, the central ring complex and nuclear filaments are inverted. The dynamic stoichiometry data was integrated to create a spatiotemporal model of the NPC assembly pathway and predict the structures of postmitotic NPC assembly intermediates.

RevDate: 2022-12-27

Li R, Song X, Gao S, et al (2022)

Analysis on the interactions between the first introns and other introns in mitochondrial ribosomal protein genes.

Frontiers in microbiology, 13:1091698.

It is realized that the first intron plays a key role in regulating gene expression, and the interactions between the first introns and other introns must be related to the regulation of gene expression. In this paper, the sequences of mitochondrial ribosomal protein genes were selected as the samples, based on the Smith-Waterman method, the optimal matched segments between the first intron and the reverse complementary sequences of other introns of each gene were obtained, and the characteristics of the optimal matched segments were analyzed. The results showed that the lengths and the ranges of length distributions of the optimal matched segments are increased along with the evolution of eukaryotes. For the distributions of the optimal matched segments with different GC contents, the peak values are decreased along with the evolution of eukaryotes, but the corresponding GC content of the peak values are increased along with the evolution of eukaryotes, it means most introns of higher organisms interact with each other though weak bonds binding. By comparing the lengths and matching rates of optimal matched segments with those of siRNA and miRNA, it is found that some optimal matched segments may be related to non-coding RNA with special biological functions, just like siRNA and miRNA, they may play an important role in the process of gene expression and regulation. For the relative position of the optimal matched segments, the peaks of relative position distributions of optimal matched segments are increased during the evolution of eukaryotes, and the positions of the first two peaks exhibit significant conservatism.

RevDate: 2023-04-05
CmpDate: 2023-04-04

Spang A (2023)

Is an archaeon the ancestor of eukaryotes?.

Environmental microbiology, 25(4):775-779.

The origin of complex cellular life is a key puzzle in evolutionary research, which has broad implications for various neighbouring scientific disciplines. Naturally, views on this topic vary widely depending on the world view and context from which this topic is approached. In the following, I will share my perspective about our current scientific knowledge on the origin of eukaryotic cells, that is, eukaryogenesis, from a biological point of view focusing on the question as to whether an archaeon was the ancestor of eukaryotes.

RevDate: 2022-12-21

Guglielmini J, Gaia M, Da Cunha V, et al (2022)

Viral origin of eukaryotic type IIA DNA topoisomerases.

Virus evolution, 8(2):veac097.

Type II DNA topoisomerases of the family A (Topo IIAs) are present in all Bacteria (DNA gyrase) and eukaryotes. In eukaryotes, they play a major role in transcription, DNA replication, chromosome segregation, and modulation of chromosome architecture. The origin of eukaryotic Topo IIA remains mysterious since they are very divergent from their bacterial homologs and have no orthologs in Archaea. Interestingly, eukaryotic Topo IIAs have close homologs in viruses of the phylum Nucleocytoviricota, an expansive assemblage of large and giant viruses formerly known as the nucleocytoplasmic large DNA viruses. Topo IIAs are also encoded by some bacterioviruses of the class Caudoviricetes (tailed bacteriophages). To elucidate the origin of the eukaryotic Topo IIA, we performed in-depth phylogenetic analyses on a dataset combining viral and cellular Topo IIA homologs. Topo IIAs encoded by Bacteria and eukaryotes form two monophyletic groups nested within Topo IIA encoded by Caudoviricetes and Nucleocytoviricota, respectively. Importantly, Nucleocytoviricota remained well separated from eukaryotes after removing both Bacteria and Caudoviricetes from the data set, indicating that the separation of Nucleocytoviricota and eukaryotes is probably not due to long-branch attraction artifact. The topologies of our trees suggest that the eukaryotic Topo IIA was probably acquired from an ancestral member of the Nucleocytoviricota of the class Megaviricetes, before the emergence of the last eukaryotic common ancestor (LECA). This result further highlights a key role of these viruses in eukaryogenesis and suggests that early proto-eukaryotes used a Topo IIB instead of a Topo IIA for solving their DNA topological problems.

RevDate: 2023-01-06
CmpDate: 2022-12-07

Cahill MA (2022)

Quo vadis PGRMC? Grand-Scale Biology in Human Health and Disease.

Frontiers in bioscience (Landmark edition), 27(11):318.

The title usage of Latin Quo vadis 'where are you going' extends the question Unde venisti from where 'did you come?' posed in the accompanying paper and extends consideration of how ancient eukaryotic and eumetazoan functions of progesterone receptor membrane component (PGRMC) proteins (PGRMC1 and PGRMC2 in mammals) could influence modern human health and disease. This paper attempts to extrapolate to modern biology in terms of extensions of hypothetical ancestral functional states from early eukaryotes and the last eumetazoan common ancestor (LEUMCA), to relativize human metabolic physiology and disease. As novel cell types and functional specializations appeared in bilaterian animals, PGRMC functions are hypothesized to have continued to be part of the toolkit used to develop new cell types and manage increasingly complex tasks such as nerve-gut-microbiome neuronal and hormonal communication. A critical role of PGRMC (as one component of a new eumetazoan genetic machinery) is proposed in LEUMCA endocrinology, neurogenesis, and nerve-gut communication with possible involvement in circadian nicotinamide adenine dinucleotide synthesis. This model would explain the contribution of PGRMC to metabolic and differentiation/behavioral changes observed in age-related diseases like diabetes, cancer and perhaps aging itself. Consistent with proposed key regulation of neurogenesis in the LEUMCA, it is argued that Alzheimer's disease is the modern pathology that most closely reflects the suite of functions related to PGRMC biology, with the 'usual suspect' pathologies possibly being downstream of PGRMC1. Hopefully, these thoughts help to signpost directions for future research.

RevDate: 2023-01-06
CmpDate: 2022-12-07

Cahill MA (2022)

Unde venisti PGRMC? Grand-Scale Biology from Early Eukaryotes and Eumetazoan Animal Origins.

Frontiers in bioscience (Landmark edition), 27(11):317.

The title usage of Unde venisti 'from where have you come' is from a now dead language (Latin) that foundationally influenced modern English (not the major influence, but an essential formative one). This is an apt analogy for how both the ancient eukaryotic and eumetazoan functions of PGRMC proteins (PGRMC1 and PGRMC2 in mammals) probably influence modern human biology: via a formative trajectory from an evolutionarily foundational fulcrum. There is an arguable probability, although not a certainty, that PGRMC-like proteins were involved in eukaryogenesis. If so, then the proto-eukaryotic ancestral protein is modelled as having initiated the oxygen-induced and CYP450 (Cytochrome P450)-mediated synthesis of sterols in the endoplasmic reticulum to regulate proto-mitochondrial activity and heme homeostasis, as well as having enabled sterol transport between endoplasmic reticulum (ER) and mitochondria membranes involving the actin cytoskeleton, transport of heme from mitochondria, and possibly the regulation/origins of mitosis/meiosis. Later, during animal evolution, the last eumetazoan common ancestor (LEUMCA) acquired PGRMC phosphorylated tyrosines coincidentally with the gastrulation organizer, Netrin/deleted in colorectal carcinoma (DCC) signaling, muscle fibers, synapsed neurons, and neural recovery via a sleep-like process. Modern PGRMC proteins regulate multiple functions, including CYP450-mediated steroidogenesis, membrane trafficking, heme homeostasis, glycolysis/Warburg effect, fatty acid metabolism, mitochondrial regulation, and genomic CpG epigenetic regulation of gene expression. The latter imposes the system of differentiation status-sensitive cell-type specific proteomic complements in multi-tissued descendants of the LEUMCA. This paper attempts to trace PGRMC functions through time, proposing that key functions were involved in early eukaryotes, and were later added upon in the LEUMCA. An accompanying paper considers the implications of this awareness for human health and disease.

RevDate: 2023-02-24
CmpDate: 2023-01-19

Ponlachantra K, Suginta W, Robinson RC, et al (2023)

AlphaFold2: A versatile tool to predict the appearance of functional adaptations in evolution: Profilin interactions in uncultured Asgard archaea: Profilin interactions in uncultured Asgard archaea.

BioEssays : news and reviews in molecular, cellular and developmental biology, 45(2):e2200119.

The release of AlphaFold2 (AF2), a deep-learning-aided, open-source protein structure prediction program, from DeepMind, opened a new era of molecular biology. The astonishing improvement in the accuracy of the structure predictions provides the opportunity to characterize protein systems from uncultured Asgard archaea, key organisms in evolutionary biology. Despite the accumulation in metagenomics-derived Asgard archaea eukaryotic-like protein sequences, limited structural and biochemical information have restricted the insight in their potential functions. In this review, we focus on profilin, an actin-dynamics regulating protein, which in eukaryotes, modulates actin polymerization through (1) direct actin interaction, (2) polyproline binding, and (3) phospholipid binding. We assess AF2-predicted profilin structures in their potential abilities to participate in these activities. We demonstrate that AF2 is a powerful new tool for understanding the emergence of biological functional traits in evolution.

RevDate: 2023-02-03
CmpDate: 2022-11-22

Field MC, MP Rout (2022)

Coatomer in the universe of cellular complexity.

Molecular biology of the cell, 33(14):.

Eukaryotic cells possess considerable internal complexity, differentiating them from prokaryotes. Eukaryogenesis, an evolutionary transitional period culminating in the last eukaryotic common ancestor (LECA), marked the origin of the eukaryotic endomembrane system. LECA is reconstructed as possessing intracellular complexity akin to modern eukaryotes. Construction of endomembrane compartments involved three key gene families: coatomer, BAR-domain proteins, and ESCRT. Each has a distinct evolutionary origin, but of these coatomer and BAR proteins are eukaryote specific, while ESCRT has more ancient origins. We discuss the structural motifs defining these three membrane-coating complexes and suggest that compared with BAR and ESCRT, the coatomer architecture had a unique ability to be readily and considerably modified, unlocking functional diversity and enabling the development of the eukaryotic cell.

RevDate: 2023-02-24
CmpDate: 2022-12-21

Mencía M (2023)

Acid digestion and symbiont: Proton sharing at the origin of mitochondriogenesis?: Proton production by a symbiotic bacterium may have been the origin of two hallmark eukaryotic features, acid digestion and mitochondria: Proton production by a symbiotic bacterium may have been the origin of two hallmark eukaryotic features, acid digestion and mitochondria.

BioEssays : news and reviews in molecular, cellular and developmental biology, 45(1):e2200136.

The initial relationships between organisms leading to endosymbiosis and the first eukaryote are currently a topic of hot debate. Here, I present a theory that offers a gradual scenario in which the origins of phagocytosis and mitochondria are intertwined in such a way that the evolution of one would not be possible without the other. In this scenario, the premitochondrial bacterial symbiont became initially associated with a protophagocytic host on the basis of cooperation to kill prey with symbiont-produced toxins and reactive oxygen species (ROS). Subsequently, the cooperation was focused on the digestion stage, through the acidification of the protophagocytic cavities via exportation of protons produced by the aerobic respiration of the symbiont. The host gained an improved phagocytic capacity and the symbiont received organic compounds from prey. As the host gradually lost its membrane energetics to develop lysosomal digestion, respiration was centralized in the premitochondrial symbiont for energy production for the consortium.

RevDate: 2023-03-21
CmpDate: 2023-03-14

van der Gulik PTS, Hoff WD, D Speijer (2023)

Renewing Linnaean taxonomy: a proposal to restructure the highest levels of the Natural System.

Biological reviews of the Cambridge Philosophical Society, 98(2):584-602.

During the last century enormous progress has been made in the understanding of biological diversity, involving a dramatic shift from macroscopic to microscopic organisms. The question now arises as to whether the Natural System introduced by Carl Linnaeus, which has served as the central system for organizing biological diversity, can accommodate the great expansion of diversity that has been discovered. Important discoveries regarding biological diversity have not been fully integrated into a formal, coherent taxonomic system. In addition, because of taxonomic challenges and conflicts, various proposals have been made to abandon key aspects of the Linnaean system. We review the current status of taxonomy of the living world, focussing on groups at the taxonomic level of phylum and above. We summarize the main arguments against and in favour of abandoning aspects of the Linnaean system. Based on these considerations, we conclude that retaining the Linnaean Natural System provides important advantages. We propose a relatively small number of amendments for extending this system, particularly to include the named rank of world (Latin alternative mundis) formally to include non-cellular entities (viruses), and the named rank of empire (Latin alternative imperium) to accommodate the depth of diversity in (unicellular) eukaryotes that has been uncovered. We argue that in the case of both the eukaryotic domain and the viruses the cladistic approach intrinsically fails. However, the resulting semi-cladistic system provides a productive way forward that can help resolve taxonomic challenges. The amendments proposed allow us to: (i) retain named taxonomic levels and the three-domain system, (ii) improve understanding of the main eukaryotic lineages, and (iii) incorporate viruses into the Natural System. Of note, the proposal described herein is intended to serve as the starting point for a broad scientific discussion regarding the modernization of the Linnaean system.

RevDate: 2022-11-16
CmpDate: 2022-11-14

Raval PK, Garg SG, SB Gould (2022)

Endosymbiotic selective pressure at the origin of eukaryotic cell biology.

eLife, 11:.

The dichotomy that separates prokaryotic from eukaryotic cells runs deep. The transition from pro- to eukaryote evolution is poorly understood due to a lack of reliable intermediate forms and definitions regarding the nature of the first host that could no longer be considered a prokaryote, the first eukaryotic common ancestor, FECA. The last eukaryotic common ancestor, LECA, was a complex cell that united all traits characterising eukaryotic biology including a mitochondrion. The role of the endosymbiotic organelle in this radical transition towards complex life forms is, however, sometimes questioned. In particular the discovery of the asgard archaea has stimulated discussions regarding the pre-endosymbiotic complexity of FECA. Here we review differences and similarities among models that view eukaryotic traits as isolated coincidental events in asgard archaeal evolution or, on the contrary, as a result of and in response to endosymbiosis. Inspecting eukaryotic traits from the perspective of the endosymbiont uncovers that eukaryotic cell biology can be explained as having evolved as a solution to housing a semi-autonomous organelle and why the addition of another endosymbiont, the plastid, added no extra compartments. Mitochondria provided the selective pressures for the origin (and continued maintenance) of eukaryotic cell complexity. Moreover, they also provided the energetic benefit throughout eukaryogenesis for evolving thousands of gene families unique to eukaryotes. Hence, a synthesis of the current data lets us conclude that traits such as the Golgi apparatus, the nucleus, autophagosomes, and meiosis and sex evolved as a response to the selective pressures an endosymbiont imposes.

RevDate: 2022-11-02

Cellier MFM (2022)

Nramp: Deprive and conquer?.

Frontiers in cell and developmental biology, 10:988866.

Solute carriers 11 (Slc11) evolved from bacterial permease (MntH) to eukaryotic antibacterial defense (Nramp) while continuously mediating proton (H[+])-dependent manganese (Mn[2+]) import. Also, Nramp horizontal gene transfer (HGT) toward bacteria led to mntH polyphyly. Prior demonstration that evolutionary rate-shifts distinguishing Slc11 from outgroup carriers dictate catalytic specificity suggested that resolving Slc11 family tree may provide a function-aware phylogenetic framework. Hence, MntH C (MC) subgroups resulted from HGTs of prototype Nramp (pNs) parologs while archetype Nramp (aNs) correlated with phagocytosis. PHI-Blast based taxonomic profiling confirmed MntH B phylogroup is confined to anaerobic bacteria vs. MntH A (MA)'s broad distribution; suggested niche-related spread of MC subgroups; established that MA-variant MH, which carries 'eukaryotic signature' marks, predominates in archaea. Slc11 phylogeny shows MH is sister to Nramp. Site-specific analysis of Slc11 charge network known to interact with the protonmotive force demonstrates sequential rate-shifts that recapitulate Slc11 evolution. 3D mapping of similarly coevolved sites across Slc11 hydrophobic core revealed successive targeting of discrete areas. The data imply that pN HGT could advantage recipient bacteria for H[+]-dependent Mn[2+] acquisition and Alphafold 3D models suggest conformational divergence among MC subgroups. It is proposed that Slc11 originated as a bacterial stress resistance function allowing Mn[2+]-dependent persistence in conditions adverse for growth, and that archaeal MH could contribute to eukaryogenesis as a Mn[2+] sequestering defense perhaps favoring intracellular growth-competent bacteria.

RevDate: 2023-05-31
CmpDate: 2022-12-16

Nachmias D, Melnikov N, Zorea A, et al (2023)

Asgard ESCRT-III and VPS4 reveal conserved chromatin binding properties of the ESCRT machinery.

The ISME journal, 17(1):117-129.

The archaeal Asgard superphylum currently stands as the most promising prokaryotic candidate, from which eukaryotic cells emerged. This unique superphylum encodes for eukaryotic signature proteins (ESP) that could shed light on the origin of eukaryotes, but the properties and function of these proteins is largely unresolved. Here, we set to understand the function of an Asgard archaeal protein family, namely the ESCRT machinery, that is conserved across all domains of life and executes basic cellular eukaryotic functions, including membrane constriction during cell division. We find that ESCRT proteins encoded in Loki archaea, express in mammalian and yeast cells, and that the Loki ESCRT-III protein, CHMP4-7, resides in the eukaryotic nucleus in both organisms. Moreover, Loki ESCRT-III proteins associated with chromatin, recruited their AAA-ATPase VPS4 counterpart to organize in discrete foci in the mammalian nucleus, and directly bind DNA. The human ESCRT-III protein, CHMP1B, exhibited similar nuclear properties and recruited both human and Asgard VPS4s to nuclear foci, indicating interspecies interactions. Mutation analysis revealed a role for the N terminal region of ESCRT-III in mediating these phenotypes in both human and Asgard ESCRTs. These findings suggest that ESCRT proteins hold chromatin binding properties that were highly preserved through the billion years of evolution separating Asgard archaea and humans. The conserved chromatin binding properties of the ESCRT membrane remodeling machinery, reported here, may have important implications for the origin of eukaryogenesis.

RevDate: 2022-12-23
CmpDate: 2022-12-02

Chen D, Zhang T, Chen Y, et al (2022)

Tree2GD: a phylogenomic method to detect large-scale gene duplication events.

Bioinformatics (Oxford, England), 38(23):5317-5321.

MOTIVATION: Whole-genome duplication events have long been discovered throughout the evolution of eukaryotes, contributing to genome complexity and biodiversity and leaving traces in the descending organisms. Therefore, an accurate and rapid phylogenomic method is needed to identify the retained duplicated genes on various lineages across the target taxonomy.

RESULTS: Here, we present Tree2GD, an integrated method to identify large-scale gene duplication events by automatically perform multiple procedures, including sequence alignment, recognition of homolog, gene tree/species tree reconciliation, Ks distribution of gene duplicates and synteny analyses. Application of Tree2GD on 2 datasets, 12 metazoan genomes and 68 angiosperms, successfully identifies all reported whole-genome duplication events exhibited by these species, showing effectiveness and efficiency of Tree2GD on phylogenomic analyses of large-scale gene duplications.

Tree2GD is written in Python and C++ and is available at

SUPPLEMENTARY INFORMATION: Supplementary data are available at Bioinformatics online.

RevDate: 2022-10-19

Silva VSD, CR Machado (2022)

Sex in protists: A new perspective on the reproduction mechanisms of trypanosomatids.

Genetics and molecular biology, 45(3):e20220065.

The Protist kingdom individuals are the most ancestral representatives of eukaryotes. They have inhabited Earth since ancient times and are currently found in the most diverse environments presenting a great heterogeneity of life forms. The unicellular and multicellular algae, photosynthetic and heterotrophic organisms, as well as free-living and pathogenic protozoa represents the protist group. The evolution of sex is directly associated with the origin of eukaryotes being protists the earliest protagonists of sexual reproduction on earth. In eukaryotes, the recombination through genetic exchange is a ubiquitous mechanism that can be stimulated by DNA damage. Scientific evidences support the hypothesis that reactive oxygen species (ROS) induced DNA damage can promote sexual recombination in eukaryotes which might have been a decisive factor for the origin of sex. The fact that some recombination enzymes also participate in meiotic sex in modern eukaryotes reinforces the idea that sexual reproduction emerged as consequence of specific mechanisms to cope with mutations and alterations in genetic material. In this review we will discuss about origin of sex and different strategies of evolve sexual reproduction in some protists such that cause human diseases like malaria, toxoplasmosis, sleeping sickness, Chagas disease, and leishmaniasis.

RevDate: 2023-01-23
CmpDate: 2022-12-28

Abrahim M, Machado E, Alvarez-Valín F, et al (2022)

Uncovering Pseudogenes and Intergenic Protein-coding Sequences in TriTryps' Genomes.

Genome biology and evolution, 14(10):.

Trypanosomatids belong to a remarkable group of unicellular, parasitic organisms of the order Kinetoplastida, an early diverging branch of the phylogenetic tree of eukaryotes, exhibiting intriguing biological characteristics affecting gene expression (intronless polycistronic transcription, trans-splicing, and RNA editing), metabolism, surface molecules, and organelles (compartmentalization of glycolysis, variation of the surface molecules, and unique mitochondrial DNA), cell biology and life cycle (phagocytic vacuoles evasion and intricate patterns of cell morphogenesis). With numerous genomic-scale data of several trypanosomatids becoming available since 2005 (genomes, transcriptomes, and proteomes), the scientific community can further investigate the mechanisms underlying these unusual features and address other unexplored phenomena possibly revealing biological aspects of the early evolution of eukaryotes. One fundamental aspect comprises the processes and mechanisms involved in the acquisition and loss of genes throughout the evolutionary history of these primitive microorganisms. Here, we present a comprehensive in silico analysis of pseudogenes in three major representatives of this group: Leishmania major, Trypanosoma brucei, and Trypanosoma cruzi. Pseudogenes, DNA segments originating from altered genes that lost their original function, are genomic relics that can offer an essential record of the evolutionary history of functional genes, as well as clues about the dynamics and evolution of hosting genomes. Scanning these genomes with functional proteins as proxies to reveal intergenic regions with protein-coding features, relying on a customized threshold to distinguish statistically and biologically significant sequence similarities, and reassembling remnant sequences from their debris, we found thousands of pseudogenes and hundreds of open reading frames, with particular characteristics in each trypanosomatid: mutation profile, number, content, density, codon bias, average size, single- or multi-copy gene origin, number and type of mutations, putative primitive function, and transcriptional activity. These features suggest a common process of pseudogene formation, different patterns of pseudogene evolution and extant biological functions, and/or distinct genome organization undertaken by those parasites during evolution, as well as different evolutionary and/or selective pressures acting on distinct lineages.

RevDate: 2023-01-23
CmpDate: 2022-10-24

Gäbelein CG, Reiter MA, Ernst C, et al (2022)

Engineering Endosymbiotic Growth of E. coli in Mammalian Cells.

ACS synthetic biology, 11(10):3388-3396.

Endosymbioses are cellular mergers in which one cell lives within another cell and have led to major evolutionary transitions, most prominently to eukaryogenesis. Generation of synthetic endosymbioses aims to provide a defined starting point for studying fundamental processes in emerging endosymbiotic systems and enable the engineering of cells with novel properties. Here, we tested the potential of different bacteria for artificial endosymbiosis in mammalian cells. To this end, we adopted the fluidic force microscopy technology to inject diverse bacteria directly into the cytosol of HeLa cells and examined the endosymbiont-host interactions by real-time fluorescence microscopy. Among them, Escherichia coli grew exponentially within the cytoplasm, however, at a faster pace than its host cell. To slow down the intracellular growth of E. coli, we introduced auxotrophies in E. coli and demonstrated that the intracellular growth rate can be reduced by limiting the uptake of aromatic amino acids. In consequence, the survival of the endosymbiont-host pair was prolonged. The presented experimental framework enables studying endosymbiotic candidate systems at high temporal resolution and at the single cell level. Our work represents a starting point for engineering a stable, vertically inherited endosymbiosis.

RevDate: 2022-09-26
CmpDate: 2022-09-23

Forterre P (2022)

Archaea: A Goldmine for Molecular Biologists and Evolutionists.

Methods in molecular biology (Clifton, N.J.), 2522:1-21.

The rebuttal of the prokaryote-eukaryote dichotomy and the elaboration of the three domains concept by Carl Woese and colleagues has been a breakthrough in biology. With the methodologies available at this time, they have shown that a single molecule, the 16S ribosomal RNA, could reveal the global organization of the living world. Later on, mining archaeal genomes led to major discoveries in archaeal molecular biology, providing a third model for comparative molecular biology. These analyses revealed the strong eukaryal flavor of the basic molecular fabric of Archaea and support rooting the universal tree between Bacteria and Arcarya (the clade grouping Archaea and Eukarya). However, in contradiction with this conclusion, it remains to understand why the archaeal and bacterial mobilomes are so similar and so different from the eukaryal one. These last years, the number of recognized archaea lineages (phyla?) has exploded. The archaeal nomenclature is now in turmoil and debates about the nature of the last universal common ancestor, the last archaeal common ancestor, and the topology of the tree of life are still going on. Interestingly, the expansion of the archaeal eukaryome, especially in the Asgard archaea, has provided new opportunities to study eukaryogenesis. In recent years, the application to Archaea of the new methodologies described in the various chapters of this book have opened exciting avenues to study the molecular biology and the physiology of these fascinating microorganisms.

RevDate: 2022-10-13
CmpDate: 2022-09-16

Tricou T, Tannier E, DM de Vienne (2022)

Ghost lineages can invalidate or even reverse findings regarding gene flow.

PLoS biology, 20(9):e3001776.

Introgression, endosymbiosis, and gene transfer, i.e., horizontal gene flow (HGF), are primordial sources of innovation in all domains of life. Our knowledge on HGF relies on detection methods that exploit some of its signatures left on extant genomes. One of them is the effect of HGF on branch lengths of constructed phylogenies. This signature has been formalized in statistical tests for HGF detection and used for example to detect massive adaptive gene flows in malaria vectors or to order evolutionary events involved in eukaryogenesis. However, these studies rely on the assumption that ghost lineages (all unsampled extant and extinct taxa) have little influence. We demonstrate here with simulations and data reanalysis that when considering the more realistic condition that unsampled taxa are legion compared to sampled ones, the conclusion of these studies become unfounded or even reversed. This illustrates the necessity to recognize the existence of ghosts in evolutionary studies.

RevDate: 2022-10-04
CmpDate: 2022-09-08

Akıl C, Tran LT, Orhant-Prioux M, et al (2022)

Structural and biochemical evidence for the emergence of a calcium-regulated actin cytoskeleton prior to eukaryogenesis.

Communications biology, 5(1):890.

Charting the emergence of eukaryotic traits is important for understanding the characteristics of organisms that contributed to eukaryogenesis. Asgard archaea and eukaryotes are the only organisms known to possess regulated actin cytoskeletons. Here, we determined that gelsolins (2DGels) from Lokiarchaeota (Loki) and Heimdallarchaeota (Heim) are capable of regulating eukaryotic actin dynamics in vitro and when expressed in eukaryotic cells. The actin filament severing and capping, and actin monomer sequestering, functionalities of 2DGels are strictly calcium controlled. We determined the X-ray structures of Heim and Loki 2DGels bound actin monomers. Each structure possesses common and distinct calcium-binding sites. Loki2DGel has an unusual WH2-like motif (LVDV) between its two gelsolin domains, in which the aspartic acid coordinates a calcium ion at the interface with actin. We conclude that the calcium-regulated actin cytoskeleton predates eukaryogenesis and emerged in the predecessors of the last common ancestor of Loki, Heim and Thorarchaeota.

RevDate: 2023-01-07
CmpDate: 2022-08-31

Kontou A, Herman EK, Field MC, et al (2022)

Evolution of factors shaping the endoplasmic reticulum.

Traffic (Copenhagen, Denmark), 23(9):462-473.

Endomembrane system compartments are significant elements in virtually all eukaryotic cells, supporting functions including protein synthesis, post-translational modifications and protein/lipid targeting. In terms of membrane area the endoplasmic reticulum (ER) is the largest intracellular organelle, but the origins of proteins defining the organelle and the nature of lineage-specific modifications remain poorly studied. To understand the evolution of factors mediating ER morphology and function we report a comparative genomics analysis of experimentally characterized ER-associated proteins involved in maintaining ER structure. We find that reticulons, REEPs, atlastins, Ufe1p, Use1p, Dsl1p, TBC1D20, Yip3p and VAPs are highly conserved, suggesting an origin at least as early as the last eukaryotic common ancestor (LECA), although many of these proteins possess additional non-ER functions in modern eukaryotes. Secondary losses are common in individual species and in certain lineages, for example lunapark is missing from the Stramenopiles and the Alveolata. Lineage-specific innovations include protrudin, Caspr1, Arl6IP1, p180, NogoR, kinectin and CLIMP-63, which are restricted to the Opisthokonta. Hence, much of the machinery required to build and maintain the ER predates the LECA, but alternative strategies for the maintenance and elaboration of ER shape and function are present in modern eukaryotes. Moreover, experimental investigations for ER maintenance factors in diverse eukaryotes are expected to uncover novel mechanisms.

RevDate: 2023-02-03
CmpDate: 2022-09-19

Obado SO, Rout MP, MC Field (2022)

Sending the message: specialized RNA export mechanisms in trypanosomes.

Trends in parasitology, 38(10):854-867.

Export of RNA from the nucleus is essential for all eukaryotic cells and has emerged as a major step in the control of gene expression. mRNA molecules are required to complete a complex series of processing events and pass a quality control system to protect the cytoplasm from the translation of aberrant proteins. Many of these events are highly conserved across eukaryotes, reflecting their ancient origin, but significant deviation from a canonical pathway as described from animals and fungi has emerged in the trypanosomatids. With significant implications for the mechanisms that control gene expression and hence differentiation, responses to altered environments and fitness as a parasite, these deviations may also reveal additional, previously unsuspected, mRNA export pathways.

RevDate: 2022-10-14
CmpDate: 2022-08-24

Colnaghi M, Lane N, A Pomiankowski (2022)

Repeat sequences limit the effectiveness of lateral gene transfer and favored the evolution of meiotic sex in early eukaryotes.

Proceedings of the National Academy of Sciences of the United States of America, 119(35):e2205041119.

The transition from prokaryotic lateral gene transfer to eukaryotic meiotic sex is poorly understood. Phylogenetic evidence suggests that it was tightly linked to eukaryogenesis, which involved an unprecedented rise in both genome size and the density of genetic repeats. Expansion of genome size raised the severity of Muller's ratchet, while limiting the effectiveness of lateral gene transfer (LGT) at purging deleterious mutations. In principle, an increase in recombination length combined with higher rates of LGT could solve this problem. Here, we show using a computational model that this solution fails in the presence of genetic repeats prevalent in early eukaryotes. The model demonstrates that dispersed repeat sequences allow ectopic recombination, which leads to the loss of genetic information and curtails the capacity of LGT to prevent mutation accumulation. Increasing recombination length in the presence of repeat sequences exacerbates the problem. Mutational decay can only be resisted with homology along extended sequences of DNA. We conclude that the transition to homologous pairing along linear chromosomes was a key innovation in meiotic sex, which was instrumental in the expansion of eukaryotic genomes and morphological complexity.

RevDate: 2022-08-04
CmpDate: 2022-07-28

Schavemaker PE, M Lynch (2022)

Flagellar energy costs across the tree of life.

eLife, 11:.

Flagellar-driven motility grants unicellular organisms the ability to gather more food and avoid predators, but the energetic costs of construction and operation of flagella are considerable. Paths of flagellar evolution depend on the deviations between fitness gains and energy costs. Using structural data available for all three major flagellar types (bacterial, archaeal, and eukaryotic), flagellar construction costs were determined for Escherichia coli, Pyrococcus furiosus, and Chlamydomonas reinhardtii. Estimates of cell volumes, flagella numbers, and flagellum lengths from the literature yield flagellar costs for another ~200 species. The benefits of flagellar investment were analysed in terms of swimming speed, nutrient collection, and growth rate; showing, among other things, that the cost-effectiveness of bacterial and eukaryotic flagella follows a common trend. However, a comparison of whole-cell costs and flagellum costs across the Tree of Life reveals that only cells with larger cell volumes than the typical bacterium could evolve the more expensive eukaryotic flagellum. These findings provide insight into the unsolved evolutionary question of why the three domains of life each carry their own type of flagellum.

RevDate: 2022-09-20
CmpDate: 2022-08-12

Cerón-Romero MA, Fonseca MM, de Oliveira Martins L, et al (2022)

Phylogenomic Analyses of 2,786 Genes in 158 Lineages Support a Root of the Eukaryotic Tree of Life between Opisthokonts and All Other Lineages.

Genome biology and evolution, 14(8):.

Advances in phylogenomics and high-throughput sequencing have allowed the reconstruction of deep phylogenetic relationships in the evolution of eukaryotes. Yet, the root of the eukaryotic tree of life remains elusive. The most popular hypothesis in textbooks and reviews is a root between Unikonta (Opisthokonta + Amoebozoa) and Bikonta (all other eukaryotes), which emerged from analyses of a single-gene fusion. Subsequent, highly cited studies based on concatenation of genes supported this hypothesis with some variations or proposed a root within Excavata. However, concatenation of genes does not consider phylogenetically-informative events like gene duplications and losses. A recent study using gene tree parsimony (GTP) suggested the root lies between Opisthokonta and all other eukaryotes, but only including 59 taxa and 20 genes. Here we use GTP with a duplication-loss model in a gene-rich and taxon-rich dataset (i.e., 2,786 gene families from two sets of 155 and 158 diverse eukaryotic lineages) to assess the root, and we iterate each analysis 100 times to quantify tree space uncertainty. We also contrasted our results and discarded alternative hypotheses from the literature using GTP and the likelihood-based method SpeciesRax. Our estimates suggest a root between Fungi or Opisthokonta and all other eukaryotes; but based on further analysis of genome size, we propose that the root between Opisthokonta and all other eukaryotes is the most likely.

RevDate: 2023-01-20
CmpDate: 2022-08-10

Romei M, Sapriel G, Imbert P, et al (2022)

Protein folds as synapomorphies of the tree of life.

Evolution; international journal of organic evolution, 76(8):1706-1719.

Several studies showed that folds (topology of protein secondary structures) distribution in proteomes may be a global proxy to build phylogeny. Then, some folds should be synapomorphies (derived characters exclusively shared among taxa). However, previous studies used methods that did not allow synapomorphy identification, which requires congruence analysis of folds as individual characters. Here, we map SCOP folds onto a sample of 210 species across the tree of life (TOL). Congruence is assessed using retention index of each fold for the TOL, and principal component analysis for deeper branches. Using a bicluster mapping approach, we define synapomorphic blocks of folds (SBF) sharing similar presence/absence patterns. Among the 1232 folds, 20% are universally present in our TOL, whereas 54% are reliable synapomorphies. These results are similar with CATH and ECOD databases. Eukaryotes are characterized by a large number of them, and several SBFs clearly support nested eukaryotic clades (divergence times from 1100 to 380 mya). Although clearly separated, the three superkingdoms reveal a strong mosaic pattern. This pattern is consistent with the dual origin of eukaryotes and witness secondary endosymbiosis in their phothosynthetic clades. Our study unveils direct analysis of folds synapomorphies as key characters to unravel evolutionary history of species.

RevDate: 2022-08-11
CmpDate: 2022-06-29

Banciu HL, Gridan IM, Zety AV, et al (2022)

Asgard archaea in saline environments.

Extremophiles : life under extreme conditions, 26(2):21.

Members of candidate Asgardarchaeota superphylum appear to share numerous eukaryotic-like attributes thus being broadly explored for their relevance to eukaryogenesis. On the contrast, the ecological roles of Asgard archaea remains understudied. Asgard archaea have been frequently associated to low-oxygen aquatic sedimentary environments worldwide spanning a broad but not extreme salinity range. To date, the available information on diversity and potential biogeochemical roles of Asgardarchaeota mostly sourced from marine habitats and to a much lesser extend from true saline environments (i.e., > 3% w/v total salinity). Here, we provide an overview on diversity and ecological implications of Asgard archaea distributed across saline environments and briefly explore their metagenome-resolved potential for osmoadaptation. Loki-, Thor- and Heimdallarchaeota are the dominant Asgard clades in saline habitats where they might employ anaerobic/microaerophilic organic matter degradation and autotrophic carbon fixation. Homologs of primary solute uptake ABC transporters seemingly prevail in Thorarchaeota, whereas those putatively involved in trehalose and ectoine biosynthesis were mostly inferred in Lokiarchaeota. We speculate that Asgardarchaeota might adopt compatible solute-accumulating ('salt-out') strategy as response to salt stress. Our current understanding on the distribution, ecology and salt-adaptive strategies of Asgardarchaeota in saline environments are, however, limited by insufficient sampling and incompleteness of the available metagenome-assembled genomes. Extensive sampling combined with 'omics'- and cultivation-based approaches seem, therefore, crucial to gain deeper knowledge on this particularly intriguing archaeal lineage.

RevDate: 2022-11-22
CmpDate: 2022-11-16

Mallén-Ponce MJ, Pérez-Pérez ME, JL Crespo (2022)

Deciphering the function and evolution of the target of rapamycin signaling pathway in microalgae.

Journal of experimental botany, 73(20):6993-7005.

Microalgae constitute a highly diverse group of photosynthetic microorganisms that are widely distributed on Earth. The rich diversity of microalgae arose from endosymbiotic events that took place early in the evolution of eukaryotes and gave rise to multiple lineages including green algae, the ancestors of land plants. In addition to their fundamental role as the primary source of marine and freshwater food chains, microalgae are essential producers of oxygen on the planet and a major biotechnological target for sustainable biofuel production and CO2 mitigation. Microalgae integrate light and nutrient signals to regulate cell growth. Recent studies identified the target of rapamycin (TOR) kinase as a central regulator of cell growth and a nutrient sensor in microalgae. TOR promotes protein synthesis and regulates processes that are induced under nutrient stress such as autophagy and the accumulation of triacylglycerol and starch. A detailed analysis of representative genomes from the entire microalgal lineage revealed that the highly conserved central components of the TOR pathway are likely to have been present in the last eukaryotic common ancestor, and the loss of specific TOR signaling elements at an early stage in the evolution of microalgae. Here we examine the evolutionary conservation of TOR signaling components in diverse microalgae and discuss recent progress of this signaling pathway in these organisms.

RevDate: 2022-10-11
CmpDate: 2022-09-13

Gophna U, N Altman-Price (2022)

Horizontal Gene Transfer in Archaea-From Mechanisms to Genome Evolution.

Annual review of microbiology, 76:481-502.

Archaea remains the least-studied and least-characterized domain of life despite its significance not just to the ecology of our planet but also to the evolution of eukaryotes. It is therefore unsurprising that research into horizontal gene transfer (HGT) in archaea has lagged behind that of bacteria. Indeed, several archaeal lineages may owe their very existence to large-scale HGT events, and thus understanding both the molecular mechanisms and the evolutionary impact of HGT in archaea is highly important. Furthermore, some mechanisms of gene exchange, such as plasmids that transmit themselves via membrane vesicles and the formation of cytoplasmic bridges that allows transfer of both chromosomal and plasmid DNA, may be archaea-specific. This review summarizes what we know about HGT in archaea, and the barriers that restrict it, highlighting exciting recent discoveries and pointing out opportunities for future research.

RevDate: 2022-10-25
CmpDate: 2022-07-13

Kumar P, Bhatnagar A, R Sankaranarayanan (2022)

Chiral proofreading during protein biosynthesis and its evolutionary implications.

FEBS letters, 596(13):1615-1627.

Homochirality of biomacromolecules is a prerequisite for their proper functioning and hence essential for all life forms. This underscores the role of cellular chiral checkpoints in enforcing homochirality during protein biosynthesis. d-Aminoacyl-tRNA deacylase (DTD) is an enzyme that performs 'chirality-based proofreading' to remove d-amino acids mistakenly attached to tRNAs, thus recycling them for further rounds of translation. Paradoxically, owing to its l-chiral rejection mode of action, DTD can remove glycine as well, which is an achiral amino acid. However, this activity is modulated by discriminator base (N73) in tRNA, a unique element that protects the cognate Gly-tRNA[Gly] . Here, we review our recent work showing various aspects of DTD and tRNA[Gly] coevolution and its key role in maintaining proper translation surveillance in both bacteria and eukaryotes. Moreover, we also discuss two major optimization events on DTD and tRNA that resolved compatibility issues among the archaeal and the bacterial translation apparatuses. Importantly, such optimizations are necessary for the emergence of mitochondria and successful eukaryogenesis.

RevDate: 2022-06-17
CmpDate: 2022-06-17

Olovnikov AM (2022)

Eco-crossover, or environmentally regulated crossing-over, and natural selection are two irreplaceable drivers of adaptive evolution: Eco-crossover hypothesis.

Bio Systems, 218:104706.

The existence of an environmentally regulated version of meiotic crossing-over, or eco-crossover, is proposed, and the main consequences of this hypothesis are considered. Eco-crossover is a key source of partially directed genetic diversity of eukaryotes. In stressful environment, it creates ecologically justified and topologically specific genetic changes, and hence phenotypic variability, with which the selection works. If variability were random, then, in the face of rapid environmental changes, natural selection could not create life-saving adaptations in a timely manner. Owing to the eco-crossover activity, epimutations, i.e., eco-dependently marked chromosomal sites, are transforming into mutations. In its work, eco-crossover uses the eco-stress-dependent versions of circular RNAs ("ecological" circRNAs), which, against the background of eco-stresses, are synthesized as variants of alternative splicing. These ecological circRNAs, binding to homologous epimutations on the homologous parent chromosomes of the meiocyte, involve them in topologically specific recombinations. These recombinations can create random mutations in nonrandom genomic sites. These quasi-random mutations serve as a pivotal source for creating all adaptations of any level of complexity. The drivers of the adaptive evolution of eukaryotes, both in micro- and macroevolution, are two irreplaceable factors - eco-crossover and natural selection.

RevDate: 2023-06-10
CmpDate: 2022-06-13

Bremer N, Tria FDK, Skejo J, et al (2022)

Ancestral State Reconstructions Trace Mitochondria But Not Phagocytosis to the Last Eukaryotic Common Ancestor.

Genome biology and evolution, 14(6):.

Two main theories have been put forward to explain the origin of mitochondria in eukaryotes: phagotrophic engulfment (undigested food) and microbial symbiosis (physiological interactions). The two theories generate mutually exclusive predictions about the order in which mitochondria and phagocytosis arose. To discriminate the alternatives, we have employed ancestral state reconstructions (ASR) for phagocytosis as a trait, phagotrophy as a feeding habit, the presence of mitochondria, the presence of plastids, and the multinucleated organization across major eukaryotic lineages. To mitigate the bias introduced by assuming a particular eukaryotic phylogeny, we reconstructed the appearance of these traits across 1789 different rooted gene trees, each having species from opisthokonts, mycetozoa, hacrobia, excavate, archeplastida, and Stramenopiles, Alveolates and Rhizaria. The trees reflect conflicting relationships and different positions of the root. We employed a novel phylogenomic test that summarizes ASR across trees which reconstructs a last eukaryotic common ancestor that possessed mitochondria, was multinucleated, lacked plastids, and was non-phagotrophic as well as non-phagocytic. This indicates that both phagocytosis and phagotrophy arose subsequent to the origin of mitochondria, consistent with findings from comparative physiology. Furthermore, our ASRs uncovered multiple origins of phagocytosis and of phagotrophy across eukaryotes, indicating that, like wings in animals, these traits are useful but neither ancestral nor homologous across groups. The data indicate that mitochondria preceded the origin of phagocytosis, such that phagocytosis cannot have been the mechanism by which mitochondria were acquired.

RevDate: 2022-07-16

Bell PJL (2022)

Eukaryogenesis: The Rise of an Emergent Superorganism.

Frontiers in microbiology, 13:858064.

Although it is widely taught that all modern life descended via modification from a last universal common ancestor (LUCA), this dominant paradigm is yet to provide a generally accepted explanation for the chasm in design between prokaryotic and eukaryotic cells. Counter to this dominant paradigm, the viral eukaryogenesis (VE) hypothesis proposes that the eukaryotes originated as an emergent superorganism and thus did not evolve from LUCA via descent with incremental modification. According to the VE hypothesis, the eukaryotic nucleus descends from a viral factory, the mitochondrion descends from an enslaved alpha-proteobacteria and the cytoplasm and plasma membrane descend from an archaeal host. A virus initiated the eukaryogenesis process by colonising an archaeal host to create a virocell that had its metabolism reprogrammed to support the viral factory. Subsequently, viral processes facilitated the entry of a bacterium into the archaeal cytoplasm which was also eventually reprogrammed to support the viral factory. As the viral factory increased control of the consortium, the archaeal genome was lost, the bacterial genome was greatly reduced and the viral factory eventually evolved into the nucleus. It is proposed that the interaction between these three simple components generated a superorganism whose emergent properties allowed the evolution of eukaryotic complexity. If the radical tenets of the VE hypothesis are ultimately accepted, current biological paradigms regarding viruses, cell theory, LUCA and the universal Tree of Life (ToL) should be fundamentally altered or completely abandoned.

RevDate: 2023-09-16
CmpDate: 2022-05-23

Vosseberg J, Schinkel M, Gremmen S, et al (2022)

The spread of the first introns in proto-eukaryotic paralogs.

Communications biology, 5(1):476.

Spliceosomal introns are a unique feature of eukaryotic genes. Previous studies have established that many introns were present in the protein-coding genes of the last eukaryotic common ancestor (LECA). Intron positions shared between genes that duplicated before LECA could in principle provide insight into the emergence of the first introns. In this study we use ancestral intron position reconstructions in two large sets of duplicated families to systematically identify these ancient paralogous intron positions. We found that 20-35% of introns inferred to have been present in LECA were shared between paralogs. These shared introns, which likely preceded ancient duplications, were wide spread across different functions, with the notable exception of nuclear transport. Since we observed a clear signal of pervasive intron loss prior to LECA, it is likely that substantially more introns were shared at the time of duplication than we can detect in LECA. The large extent of shared introns indicates an early origin of introns during eukaryogenesis and suggests an early origin of a nuclear structure, before most of the other complex eukaryotic features were established.

RevDate: 2022-11-13
CmpDate: 2022-07-13

Camus MF, Alexander-Lawrie B, Sharbrough J, et al (2022)

Inheritance through the cytoplasm.

Heredity, 129(1):31-43.

Most heritable information in eukaryotic cells is encoded in the nuclear genome, with inheritance patterns following classic Mendelian segregation. Genomes residing in the cytoplasm, however, prove to be a peculiar exception to this rule. Cytoplasmic genetic elements are generally maternally inherited, although there are several exceptions where these are paternally, biparentally or doubly-uniparentally inherited. In this review, we examine the diversity and peculiarities of cytoplasmically inherited genomes, and the broad evolutionary consequences that non-Mendelian inheritance brings. We first explore the origins of vertical transmission and uniparental inheritance, before detailing the vast diversity of cytoplasmic inheritance systems across Eukaryota. We then describe the evolution of genomic organisation across lineages, how this process has been shaped by interactions with the nuclear genome and population genetics dynamics. Finally, we discuss how both nuclear and cytoplasmic genomes have evolved to co-inhabit the same host cell via one of the longest symbiotic processes, and all the opportunities for intergenomic conflict that arise due to divergence in inheritance patterns. In sum, we cannot understand the evolution of eukaryotes without understanding hereditary symbiosis.

RevDate: 2022-11-12
CmpDate: 2022-05-11

Mills DB, Boyle RA, Daines SJ, et al (2022)

Eukaryogenesis and oxygen in Earth history.

Nature ecology & evolution, 6(5):520-532.

The endosymbiotic origin of mitochondria during eukaryogenesis has long been viewed as an adaptive response to the oxygenation of Earth's surface environment, presuming a fundamentally aerobic lifestyle for the free-living bacterial ancestors of mitochondria. This oxygen-centric view has been robustly challenged by recent advances in the Earth and life sciences. While the permanent oxygenation of the atmosphere above trace concentrations is now thought to have occurred 2.2 billion years ago, large parts of the deep ocean remained anoxic until less than 0.5 billion years ago. Neither fossils nor molecular clocks correlate the origin of mitochondria, or eukaryogenesis more broadly, to either of these planetary redox transitions. Instead, mitochondria-bearing eukaryotes are consistently dated to between these two oxygenation events, during an interval of pervasive deep-sea anoxia and variable surface-water oxygenation. The discovery and cultivation of the Asgard archaea has reinforced metabolic evidence that eukaryogenesis was initially mediated by syntrophic H2 exchange between an archaeal host and an α-proteobacterial symbiont living under anoxia. Together, these results temporally, spatially and metabolically decouple the earliest stages of eukaryogenesis from the oxygen content of the surface ocean and atmosphere. Rather than reflecting the ancestral metabolic state, obligate aerobiosis in eukaryotes is most probably derived, having only become globally widespread over the past 1 billion years as atmospheric oxygen approached modern levels.

RevDate: 2022-09-13
CmpDate: 2022-04-12

Meyer BH, Adam PS, Wagstaff BA, et al (2022)

Agl24 is an ancient archaeal homolog of the eukaryotic N-glycan chitobiose synthesis enzymes.

eLife, 11:.

Protein N-glycosylation is a post-translational modification found in organisms of all domains of life. The crenarchaeal N-glycosylation begins with the synthesis of a lipid-linked chitobiose core structure, identical to that in Eukaryotes, although the enzyme catalyzing this reaction remains unknown. Here, we report the identification of a thermostable archaeal β-1,4-N-acetylglucosaminyltransferase, named archaeal glycosylation enzyme 24 (Agl24), responsible for the synthesis of the N-glycan chitobiose core. Biochemical characterization confirmed its function as an inverting β-D-GlcNAc-(1→4)-α-D-GlcNAc-diphosphodolichol glycosyltransferase. Substitution of a conserved histidine residue, found also in the eukaryotic and bacterial homologs, demonstrated its functional importance for Agl24. Furthermore, bioinformatics and structural modeling revealed similarities of Agl24 to the eukaryotic Alg14/13 and a distant relation to the bacterial MurG, which are catalyzing the same or a similar reaction, respectively. Phylogenetic analysis of Alg14/13 homologs indicates that they are ancient in Eukaryotes, either as a lateral transfer or inherited through eukaryogenesis.

RevDate: 2023-04-03
CmpDate: 2022-04-06

Akıl C, Ali S, Tran LT, et al (2022)

Structure and dynamics of Odinarchaeota tubulin and the implications for eukaryotic microtubule evolution.

Science advances, 8(12):eabm2225.

Tubulins are critical for the internal organization of eukaryotic cells, and understanding their emergence is an important question in eukaryogenesis. Asgard archaea are the closest known prokaryotic relatives to eukaryotes. Here, we elucidated the apo and nucleotide-bound x-ray structures of an Asgard tubulin from hydrothermal living Odinarchaeota (OdinTubulin). The guanosine 5'-triphosphate (GTP)-bound structure resembles a microtubule protofilament, with GTP bound between subunits, coordinating the "+" end subunit through a network of water molecules and unexpectedly by two cations. A water molecule is located suitable for GTP hydrolysis. Time course crystallography and electron microscopy revealed conformational changes on GTP hydrolysis. OdinTubulin forms tubules at high temperatures, with short curved protofilaments coiling around the tubule circumference, more similar to FtsZ, rather than running parallel to its length, as in microtubules. Thus, OdinTubulin represents an evolutionary stage intermediate between prokaryotic FtsZ and eukaryotic microtubule-forming tubulins.

RevDate: 2022-04-08
CmpDate: 2022-04-08

Wu X, Han J, C Guo (2022)

Function of Nuclear Pore Complexes in Regulation of Plant Defense Signaling.

International journal of molecular sciences, 23(6):.

In eukaryotes, the nucleus is the regulatory center of cytogenetics and metabolism, and it is critical for fundamental biological processes, including DNA replication and transcription, protein synthesis, and biological macromolecule transportation. The eukaryotic nucleus is surrounded by a lipid bilayer called the nuclear envelope (NE), which creates a microenvironment for sophisticated cellular processes. The NE is perforated by the nuclear pore complex (NPC), which is the channel for biological macromolecule bi-directional transport between the nucleus and cytoplasm. It is well known that NPC is the spatial designer of the genome and the manager of genomic function. Moreover, the NPC is considered to be a platform for the continual adaptation and evolution of eukaryotes. So far, a number of nucleoporins required for plant-defense processes have been identified. Here, we first provide an overview of NPC organization in plants, and then discuss recent findings in the plant NPC to elaborate on and dissect the distinct defensive functions of different NPC subcomponents in plant immune defense, growth and development, hormone signaling, and temperature response. Nucleoporins located in different components of NPC have their unique functions, and the link between the NPC and nucleocytoplasmic trafficking promotes crosstalk of different defense signals in plants. It is necessary to explore appropriate components of the NPC as potential targets for the breeding of high-quality and broad spectrum resistance crop varieties.

RevDate: 2022-07-16
CmpDate: 2022-04-13

Jüttner M, S Ferreira-Cerca (2022)

Looking through the Lens of the Ribosome Biogenesis Evolutionary History: Possible Implications for Archaeal Phylogeny and Eukaryogenesis.

Molecular biology and evolution, 39(4):.

Our understanding of microbial diversity and its evolutionary relationships has increased substantially over the last decade. Such an understanding has been greatly fueled by culture-independent metagenomics analyses. However, the outcome of some of these studies and their biological and evolutionary implications, such as the origin of the eukaryotic lineage from the recently discovered archaeal Asgard superphylum, is debated. The sequences of the ribosomal constituents are amongst the most used phylogenetic markers. However, the functional consequences underlying the analysed sequence diversity and their putative evolutionary implications are essentially not taken into consideration. Here, we propose to exploit additional functional hallmarks of ribosome biogenesis to help disentangle competing evolutionary hypotheses. Using selected examples, such as the multiple origins of halophily in archaea or the evolutionary relationship between the Asgard archaea and Eukaryotes, we illustrate and discuss how function-aware phylogenetic framework can contribute to refining our understanding of archaeal phylogeny and the origin of eukaryotic cells.

RevDate: 2022-07-25
CmpDate: 2022-06-08

Spang A, Mahendrarajah TA, Offre P, et al (2022)

Evolving Perspective on the Origin and Diversification of Cellular Life and the Virosphere.

Genome biology and evolution, 14(6):.

The tree of life (TOL) is a powerful framework to depict the evolutionary history of cellular organisms through time, from our microbial origins to the diversification of multicellular eukaryotes that shape the visible biosphere today. During the past decades, our perception of the TOL has fundamentally changed, in part, due to profound methodological advances, which allowed a more objective approach to studying organismal and viral diversity and led to the discovery of major new branches in the TOL as well as viral lineages. Phylogenetic and comparative genomics analyses of these data have, among others, revolutionized our understanding of the deep roots and diversity of microbial life, the origin of the eukaryotic cell, eukaryotic diversity, as well as the origin, and diversification of viruses. In this review, we provide an overview of some of the recent discoveries on the evolutionary history of cellular organisms and their viruses and discuss a variety of complementary techniques that we consider crucial for making further progress in our understanding of the TOL and its interconnection with the virosphere.

RevDate: 2022-07-28

Albers S, Ashmore J, Pollard T, et al (2022)

Origin of eukaryotes: What can be learned from the first successfully isolated Asgard archaeon.

Faculty reviews, 11:3.

The origin of cellular complexity characterizing eukaryotic cells remains a central unresolved issue in the study of diversification of cellular life on Earth. The isolation by Imachi et al.[1] of a member of the Asgard archaea[2] - a contemporary relative of organisms thought to have given rise to eukaryotic cells about 2 billion years ago - now promises new insight. The complete genome sequence of the isolated Lokiarchaeum strain confirms that the eukaryotic signature proteins (ESPs) previously identified in the Lokiarchaeota[3] and other Asgard archaea[2] are indeed encoded by these archaeal genomes and do not represent contamination from eukaryotes. These ESPs encode homologs of eukaryotic actins, small GTPases and the ESCRT complex proteins and are required for the functioning of complex eukaryotic cells. The new, slowly growing, anaerobic laboratory strain allows a first direct look at these organisms and provides key insights into the morphology and metabolism of an Asgard archaeal organism. The work has provided valuable information for other laboratories that aim to isolate and characterize related organisms from other environments.

RevDate: 2022-04-01
CmpDate: 2022-03-31

Hugoson E, Guliaev A, Ammunét T, et al (2022)

Host Adaptation in Legionellales Is 1.9 Ga, Coincident with Eukaryogenesis.

Molecular biology and evolution, 39(3):.

Bacteria adapting to living in a host cell caused the most salient events in the evolution of eukaryotes, namely the seminal fusion with an archaeon, and the emergence of both mitochondrion and chloroplast. A bacterial clade that may hold the key to understanding these events is the deep-branching gammaproteobacterial order Legionellales-containing among others Coxiella and Legionella-of which all known members grow inside eukaryotic cells. Here, by analyzing 35 novel Legionellales genomes mainly acquired through metagenomics, we show that this group is much more diverse than previously thought, and that key host-adaptation events took place very early in its evolution. Crucial virulence factors like the Type IVB secretion (Dot/Icm) system and two shared effector proteins were gained in the last Legionellales common ancestor (LLCA). Many metabolic gene families were lost in LLCA and its immediate descendants, including functions directly and indirectly related to molybdenum metabolism. On the other hand, genome sizes increased in the ancestors of the Legionella genus. We estimate that LLCA lived approximately 1.89 Ga, probably predating the last eukaryotic common ancestor by approximately 0.4-1.0 Gy. These elements strongly indicate that host adaptation arose only once in Legionellales, and that these bacteria were using advanced molecular machinery to exploit and manipulate host cells early in eukaryogenesis.

RevDate: 2022-02-16

Medina-Chávez NO, M Travisano (2021)

Archaeal Communities: The Microbial Phylogenomic Frontier.

Frontiers in genetics, 12:693193.

Archaea are a unique system for investigating the diversity of life. There are the most diverse group of organisms with the longest evolutionary history of life on Earth. Phylogenomic investigations reveal the complex evolutionary history of Archaea, overturning longstanding views of the history of life. They exist in the harshest environments and benign conditions, providing a system to investigate the basis for living in extreme environments. They are frequently members of microbial communities, albeit generally rare. Archaea were central in the evolution of Eukaryotes and can be used as a proxy for studying life on other planets. Future advances will depend not only upon phylogenomic studies but also on a better understanding of isolation and cultivation techniques.

RevDate: 2022-04-01
CmpDate: 2022-03-31

Da Cunha V, Gaia M, Ogata H, et al (2022)

Giant Viruses Encode Actin-Related Proteins.

Molecular biology and evolution, 39(2):.

The emergence of the eukaryotic cytoskeleton is a critical yet puzzling step of eukaryogenesis. Actin and actin-related proteins (ARPs) are ubiquitous components of this cytoskeleton. The gene repertoire of the Last Eukaryotic Common Ancestor (LECA) would have therefore harbored both actin and various ARPs. Here, we report the presence and expression of actin-related genes in viral genomes (viractins) of some Imitervirales, a viral order encompassing the giant Mimiviridae. Phylogenetic analyses suggest an early recruitment of an actin-related gene by viruses from ancient protoeukaryotic hosts before the emergence of modern eukaryotes, possibly followed by a back transfer that gave rise to eukaryotic actins. This supports a coevolutionary scenario between pre-LECA lineages and their viruses, which could have contributed to the emergence of the modern eukaryotic cytoskeleton.

RevDate: 2022-05-10
CmpDate: 2022-05-10

La SR, Ndhlovu A, PM Durand (2022)

The Ancient Origins of Death Domains Support the 'Original Sin' Hypothesis for the Evolution of Programmed Cell Death.

Journal of molecular evolution, 90(1):95-113.

The discovery of caspase homologs in bacteria highlighted the relationship between programmed cell death (PCD) evolution and eukaryogenesis. However, the origin of PCD genes in prokaryotes themselves (bacteria and archaea) is poorly understood and a source of controversy. Whether archaea also contain C14 peptidase enzymes and other death domains is largely unknown because of a historical dearth of genomic data. Archaeal genomic databases have grown significantly in the last decade, which allowed us to perform a detailed comparative study of the evolutionary histories of PCD-related death domains in major archaeal phyla, including the deepest branching phyla of Candidatus Aenigmarchaeota, Candidatus Woesearchaeota, and Euryarchaeota. We identified death domains associated with executioners of PCD, like the caspase homologs of the C14 peptidase family, in 321 archaea sequences. Of these, 15.58% were metacaspase type I orthologues and 84.42% were orthocaspases. Maximum likelihood phylogenetic analyses revealed a scattered distribution of orthocaspases and metacaspases in deep-branching bacteria and archaea. The tree topology was incongruent with the prokaryote 16S phylogeny suggesting a common ancestry of PCD genes in prokaryotes and subsequent massive horizontal gene transfer coinciding with the divergence of archaea and bacteria. Previous arguments for the origin of PCD were philosophical in nature with two popular propositions being the "addiction" and 'original sin' hypotheses. Our data support the 'original sin' hypothesis, which argues for a pleiotropic origin of the PCD toolkit with pro-life and pro-death functions tracing back to the emergence of cellular life-the Last Universal Common Ancestor State.

RevDate: 2022-11-06
CmpDate: 2022-03-16

Muñoz-Gómez SA, Susko E, Williamson K, et al (2022)

Site-and-branch-heterogeneous analyses of an expanded dataset favour mitochondria as sister to known Alphaproteobacteria.

Nature ecology & evolution, 6(3):253-262.

Determining the phylogenetic origin of mitochondria is key to understanding the ancestral mitochondrial symbiosis and its role in eukaryogenesis. However, the precise evolutionary relationship between mitochondria and their closest bacterial relatives remains hotly debated. The reasons include pervasive phylogenetic artefacts as well as limited protein and taxon sampling. Here we developed a new model of protein evolution that accommodates both across-site and across-branch compositional heterogeneity. We applied this site-and-branch-heterogeneous model (MAM60 + GFmix) to a considerably expanded dataset that comprises 108 mitochondrial proteins of alphaproteobacterial origin, and novel metagenome-assembled genomes from microbial mats, microbialites and sediments. The MAM60 + GFmix model fits the data much better and agrees with analyses of compositionally homogenized datasets with conventional site-heterogenous models. The consilience of evidence thus suggests that mitochondria are sister to the Alphaproteobacteria to the exclusion of MarineProteo1 and Magnetococcia. We also show that the ancestral presence of the crista-developing mitochondrial contact site and cristae organizing system (a mitofilin-domain-containing Mic60 protein) in mitochondria and the Alphaproteobacteria only supports their close relationship.

RevDate: 2022-11-06
CmpDate: 2022-02-22

Wu F, Speth DR, Philosof A, et al (2022)

Unique mobile elements and scalable gene flow at the prokaryote-eukaryote boundary revealed by circularized Asgard archaea genomes.

Nature microbiology, 7(2):200-212.

Eukaryotic genomes are known to have garnered innovations from both archaeal and bacterial domains but the sequence of events that led to the complex gene repertoire of eukaryotes is largely unresolved. Here, through the enrichment of hydrothermal vent microorganisms, we recovered two circularized genomes of Heimdallarchaeum species that belong to an Asgard archaea clade phylogenetically closest to eukaryotes. These genomes reveal diverse mobile elements, including an integrative viral genome that bidirectionally replicates in a circular form and aloposons, transposons that encode the 5,000 amino acid-sized proteins Otus and Ephialtes. Heimdallaechaeal mobile elements have garnered various genes from bacteria and bacteriophages, likely playing a role in shuffling functions across domains. The number of archaea- and bacteria-related genes follow strikingly different scaling laws in Asgard archaea, exhibiting a genome size-dependent ratio and a functional division resembling the bacteria- and archaea-derived gene repertoire across eukaryotes. Bacterial gene import has thus likely been a continuous process unaltered by eukaryogenesis and scaled up through genome expansion. Our data further highlight the importance of viewing eukaryogenesis in a pan-Asgard context, which led to the proposal of a conceptual framework, that is, the Heimdall nucleation-decentralized innovation-hierarchical import model that accounts for the emergence of eukaryotic complexity.

RevDate: 2022-10-23
CmpDate: 2022-01-25

Sforna MC, Loron CC, Demoulin CF, et al (2022)

Intracellular bound chlorophyll residues identify 1 Gyr-old fossils as eukaryotic algae.

Nature communications, 13(1):146.

The acquisition of photosynthesis is a fundamental step in the evolution of eukaryotes. However, few phototrophic organisms are unambiguously recognized in the Precambrian record. The in situ detection of metabolic byproducts in individual microfossils is the key for the direct identification of their metabolisms. Here, we report a new integrative methodology using synchrotron-based X-ray fluorescence and absorption. We evidence bound nickel-geoporphyrins moieties in low-grade metamorphic rocks, preserved in situ within cells of a ~1 Gyr-old multicellular eukaryote, Arctacellularia tetragonala. We identify these moieties as chlorophyll derivatives, indicating that A. tetragonala was a phototrophic eukaryote, one of the first unambiguous algae. This new approach, applicable to overmature rocks, creates a strong new proxy to understand the evolution of phototrophy and diversification of early ecosystems.

RevDate: 2022-10-20
CmpDate: 2022-02-22

Bellinger MR, Wei J, Hartmann U, et al (2022)

Conservation of magnetite biomineralization genes in all domains of life and implications for magnetic sensing.

Proceedings of the National Academy of Sciences of the United States of America, 119(3):.

Animals use geomagnetic fields for navigational cues, yet the sensory mechanism underlying magnetic perception remains poorly understood. One idea is that geomagnetic fields are physically transduced by magnetite crystals contained inside specialized receptor cells, but evidence for intracellular, biogenic magnetite in eukaryotes is scant. Certain bacteria produce magnetite crystals inside intracellular compartments, representing the most ancient form of biomineralization known and having evolved prior to emergence of the crown group of eukaryotes, raising the question of whether magnetite biomineralization in eukaryotes and prokaryotes might share a common evolutionary history. Here, we discover that salmonid olfactory epithelium contains magnetite crystals arranged in compact clusters and determine that genes differentially expressed in magnetic olfactory cells, contrasted to nonmagnetic olfactory cells, share ancestry with an ancient prokaryote magnetite biomineralization system, consistent with exaptation for use in eukaryotic magnetoreception. We also show that 11 prokaryote biomineralization genes are universally present among a diverse set of eukaryote taxa and that nine of those genes are present within the Asgard clade of archaea Lokiarchaeota that affiliates with eukaryotes in phylogenomic analysis. Consistent with deep homology, we present an evolutionary genetics hypothesis for magnetite formation among eukaryotes to motivate convergent approaches for examining magnetite-based magnetoreception, molecular origins of matrix-associated biomineralization processes, and eukaryogenesis.

RevDate: 2022-04-25
CmpDate: 2022-04-25

Aouad M, Flandrois JP, Jauffrit F, et al (2022)

A divide-and-conquer phylogenomic approach based on character supermatrices resolves early steps in the evolution of the Archaea.

BMC ecology and evolution, 22(1):1.

BACKGROUND: The recent rise in cultivation-independent genome sequencing has provided key material to explore uncharted branches of the Tree of Life. This has been particularly spectacular concerning the Archaea, projecting them at the center stage as prominently relevant to understand early stages in evolution and the emergence of fundamental metabolisms as well as the origin of eukaryotes. Yet, resolving deep divergences remains a challenging task due to well-known tree-reconstruction artefacts and biases in extracting robust ancient phylogenetic signal, notably when analyzing data sets including the three Domains of Life. Among the various strategies aimed at mitigating these problems, divide-and-conquer approaches remain poorly explored, and have been primarily based on reconciliation among single gene trees which however notoriously lack ancient phylogenetic signal.

RESULTS: We analyzed sub-sets of full supermatrices covering the whole Tree of Life with specific taxonomic sampling to robustly resolve different parts of the archaeal phylogeny in light of their current diversity. Our results strongly support the existence and early emergence of two main clades, Cluster I and Cluster II, which we name Ouranosarchaea and Gaiarchaea, and we clarify the placement of important novel archaeal lineages within these two clades. However, the monophyly and branching of the fast evolving nanosized DPANN members remains unclear and worth of further study.

CONCLUSIONS: We inferred a well resolved rooted phylogeny of the Archaea that includes all recently described phyla of high taxonomic rank. This phylogeny represents a valuable reference to study the evolutionary events associated to the early steps of the diversification of the archaeal domain. Beyond the specifics of archaeal phylogeny, our results demonstrate the power of divide-and-conquer approaches to resolve deep phylogenetic relationships, which should be applied to progressively resolve the entire Tree of Life.

RevDate: 2022-03-16
CmpDate: 2022-03-16

Rand DM, Mossman JA, Spierer AN, et al (2022)

Mitochondria as environments for the nuclear genome in Drosophila: mitonuclear G×G×E.

The Journal of heredity, 113(1):37-47.

Mitochondria evolved from a union of microbial cells belonging to distinct lineages that were likely anaerobic. The evolution of eukaryotes required a massive reorganization of the 2 genomes and eventual adaptation to aerobic environments. The nutrients and oxygen that sustain eukaryotic metabolism today are processed in mitochondria through coordinated expression of 37 mitochondrial genes and over 1000 nuclear genes. This puts mitochondria at the nexus of gene-by-gene (G×G) and gene-by-environment (G×E) interactions that sustain life. Here we use a Drosophila model of mitonuclear genetic interactions to explore the notion that mitochondria are environments for the nuclear genome, and vice versa. We construct factorial combinations of mtDNA and nuclear chromosomes to test for epistatic interactions (G×G), and expose these mitonuclear genotypes to altered dietary environments to examine G×E interactions. We use development time and genome-wide RNAseq analyses to assess the relative contributions of mtDNA, nuclear chromosomes, and environmental effects on these traits (mitonuclear G×G×E). We show that the nuclear transcriptional response to alternative mitochondrial "environments" (G×G) has significant overlap with the transcriptional response of mitonuclear genotypes to altered dietary environments. These analyses point to specific transcription factors (e.g., giant) that mediated these interactions, and identified coexpressed modules of genes that may account for the overlap in differentially expressed genes. Roughly 20% of the transcriptome includes G×G genes that are concordant with G×E genes, suggesting that mitonuclear interactions are part of an organism's environment.

RevDate: 2022-04-05
CmpDate: 2022-04-05

Cohen PA, RB Kodner (2022)

The earliest history of eukaryotic life: uncovering an evolutionary story through the integration of biological and geological data.

Trends in ecology & evolution, 37(3):246-256.

While there is significant data on eukaryogenesis and the early development of the eukaryotic lineage, major uncertainties regarding their origins and evolution remain, including questions of taxonomy, timing, and paleoecology. Here we examine the origin and diversification of the eukaryotes in the Proterozoic Eon as viewed through fossils, organic biomarkers, molecular clocks, phylogenies, and redox proxies. Our interpretation of the integration of these data suggest that eukaryotes were likely aerobic and established in Proterozoic ecosystems. We argue that we must closely examine and integrate both biological and geological evidence and examine points of agreement and contention to gain new insights into the true origin and early evolutionary history of this vastly important group.

RevDate: 2022-11-10
CmpDate: 2022-11-10

Nobs SJ, MacLeod FI, Wong HL, et al (2022)

Eukarya the chimera: eukaryotes, a secondary innovation of the two domains of life?.

Trends in microbiology, 30(5):421-431.

One of the most significant events in the evolution of life is the origin of the eukaryotic cell, an increase in cellular complexity that occurred approximately 2 billion years ago. Ground-breaking research has centered around unraveling the characteristics of the Last Eukaryotic Common Ancestor (LECA) and the nuanced archaeal and bacterial contributions in eukaryogenesis, resulting in fundamental changes in our understanding of the Tree of Life. The archaeal and bacterial roles are covered by theories of endosymbiogenesis wherein an ancestral host archaeon and a bacterial endosymbiont merged to create a new complex cell type - Eukarya - and its mitochondrion. Eukarya is often regarded as a unique and distinct domain due to complex innovations not found in archaea or bacteria, despite housing a chimeric genome containing genes of both archaeal and bacterial origin. However, the discovery of complex cell machineries in recently described Asgard archaeal lineages, and the growing support for diverse bacterial gene transfers prior to and during the time of LECA, is redefining our understanding of eukaryogenesis. Indeed, the uniqueness of Eukarya, as a domain, is challenged. It is likely that many microbial syntrophies, encompassing a 'microbial village', were required to 'raise' a eukaryote during the process of eukaryogenesis.

RevDate: 2021-12-21
CmpDate: 2021-12-21

Borao S, Ayté J, S Hümmer (2021)

Evolution of the Early Spliceosomal Complex-From Constitutive to Regulated Splicing.

International journal of molecular sciences, 22(22):.

Pre-mRNA splicing is a major process in the regulated expression of genes in eukaryotes, and alternative splicing is used to generate different proteins from the same coding gene. Splicing is a catalytic process that removes introns and ligates exons to create the RNA sequence that codifies the final protein. While this is achieved in an autocatalytic process in ancestral group II introns in prokaryotes, the spliceosome has evolved during eukaryogenesis to assist in this process and to finally provide the opportunity for intron-specific splicing. In the early stage of splicing, the RNA 5' and 3' splice sites must be brought within proximity to correctly assemble the active spliceosome and perform the excision and ligation reactions. The assembly of this first complex, termed E-complex, is currently the least understood process. We focused in this review on the formation of the E-complex and compared its composition and function in three different organisms. We highlight the common ancestral mechanisms in S. cerevisiae, S. pombe, and mammals and conclude with a unifying model for intron definition in constitutive and regulated co-transcriptional splicing.

RevDate: 2022-07-08
CmpDate: 2022-04-06

Wang L, Yang J, Zhang H, et al (2022)

Sequence coverage required for accurate genotyping by sequencing in polyploid species.

Molecular ecology resources, 22(4):1417-1426.

Polyploidy plays an important role in the evolution of eukaryotes, especially for flowering plants. Many of ecologically or agronomically important plant or crop species are polyploids, including sycamore maple (tetraploid), the world second and third largest food crops wheat (hexaploid) and potato (tetraploid) as well as economically important aquaculture animals such as Atlantic salmon and trout. The next generation sequencing data enables to allocate genotype at a sequence variant site, known as genotyping by sequencing (GBS). GBS has stimulated enormous interests in population based genomics studies in almost all diploid and many polyploid organisms. DNA sequence polymorphisms are codominant and thus fully informative about the underlying genotype at the polymorphic site, making GBS a straightforward task in diploids. However, sequence data may usually be uninformative in polyploid species, making GBS a far more challenging task in polyploids. This paper presents novel and rigorous statistical methods for predicting the number of sequence reads needed to ensure accurate GBS at a polymorphic site bared by the reads in polyploids and shows that a dozen of reads can ensure a probability of 95% to recover all constituent alleles of any tetraploid genotype but several hundreds of reads are needed to accurately uncover the genotype with probability confidence of 90%, subverting the proposition of GBS using low coverage sequence data in the literature. The theoretical prediction was tested by use of RAD-seq data from tetraploid potato cultivars. The paper provides polyploid experimentalists with theoretical guides and methods for designing and conducting their sequence-based studies.

RevDate: 2022-03-23
CmpDate: 2022-03-23

Kořený L, Oborník M, Horáková E, et al (2022)

The convoluted history of haem biosynthesis.

Biological reviews of the Cambridge Philosophical Society, 97(1):141-162.

The capacity of haem to transfer electrons, bind diatomic gases, and catalyse various biochemical reactions makes it one of the essential biomolecules on Earth and one that was likely used by the earliest forms of cellular life. Since the description of haem biosynthesis, our understanding of this multi-step pathway has been almost exclusively derived from a handful of model organisms from narrow taxonomic contexts. Recent advances in genome sequencing and functional studies of diverse and previously neglected groups have led to discoveries of alternative routes of haem biosynthesis that deviate from the 'classical' pathway. In this review, we take an evolutionarily broad approach to illuminate the remarkable diversity and adaptability of haem synthesis, from prokaryotes to eukaryotes, showing the range of strategies that organisms employ to obtain and utilise haem. In particular, the complex evolutionary histories of eukaryotes that involve multiple endosymbioses and horizontal gene transfers are reflected in the mosaic origin of numerous metabolic pathways with haem biosynthesis being a striking case. We show how different evolutionary trajectories and distinct life strategies resulted in pronounced tensions and differences in the spatial organisation of the haem biosynthesis pathway, in some cases leading to a complete loss of a haem-synthesis capacity and, rarely, even loss of a requirement for haem altogether.

RevDate: 2022-04-01
CmpDate: 2022-03-28

Petrů M, Dohnálek V, Füssy Z, et al (2021)

Fates of Sec, Tat, and YidC Translocases in Mitochondria and Other Eukaryotic Compartments.

Molecular biology and evolution, 38(12):5241-5254.

Formation of mitochondria by the conversion of a bacterial endosymbiont was a key moment in the evolution of eukaryotes. It was made possible by outsourcing the endosymbiont's genetic control to the host nucleus, while developing the import machinery for proteins synthesized on cytosolic ribosomes. The original protein export machines of the nascent organelle remained to be repurposed or were completely abandoned. This review follows the evolutionary fates of three prokaryotic inner membrane translocases Sec, Tat, and YidC. Homologs of all three translocases can still be found in current mitochondria, but with different importance for mitochondrial function. Although the mitochondrial YidC homolog, Oxa1, became an omnipresent independent insertase, the other two remained only sporadically present in mitochondria. Only a single substrate is known for the mitochondrial Tat and no function has yet been assigned for the mitochondrial Sec. Finally, this review compares these ancestral mitochondrial proteins with their paralogs operating in the plastids and the endomembrane system.

RevDate: 2022-05-13
CmpDate: 2022-04-12

Xie R, Wang Y, Huang D, et al (2022)

Expanding Asgard members in the domain of Archaea sheds new light on the origin of eukaryotes.

Science China. Life sciences, 65(4):818-829.

The hypothesis that eukaryotes originated from within the domain Archaea has been strongly supported by recent phylogenomic analyses placing Heimdallarchaeota-Wukongarchaeota branch from the Asgard superphylum as the closest known archaeal sister-group to eukaryotes. However, our understanding is still limited in terms of the relationship between eukaryotes and archaea, as well as the evolution and ecological functions of the Asgard archaea. Here, we describe three previously unknown phylum-level Asgard archaeal lineages, tentatively named Sigyn-, Freyr- and Njordarchaeota. Additional members in Wukongarchaeota and Baldrarchaeota from distinct environments are also reported here, further expanding their ecological roles and metabolic capacities. Comprehensive phylogenomic analyses further supported the origin of eukaryotes within Asgard archaea and a new lineage Njordarchaeota was supposed as the known closest branch with the eukaryotic nuclear host lineage. Metabolic reconstruction suggests that Njordarchaeota may have a heterotrophic lifestyle with capability of peptides and amino acids utilization, while Sigynarchaeota and Freyrarchaeota also have the potentials to fix inorganic carbon via the Wood-Ljungdahl pathway and degrade organic matters. Additionally, the Ack/Pta pathway for homoacetogenesis and de novo anaerobic cobalamin biosynthesis pathway were found in Freyrarchaeota and Wukongrarchaeota, respectively. Some previously unidentified eukaryotic signature proteins for intracellular membrane trafficking system, and the homologue of mu/sigma subunit of adaptor protein complex, were identified in Freyrarchaeota. This study expands the Asgard superphylum, sheds new light on the evolution of eukaryotes and improves our understanding of ecological functions of the Asgard archaea.

RevDate: 2022-03-21
CmpDate: 2022-03-21

Gabaldón T (2021)

Origin and Early Evolution of the Eukaryotic Cell.

Annual review of microbiology, 75:631-647.

The origin of eukaryotes has been defined as the major evolutionary transition since the origin of life itself. Most hallmark traits of eukaryotes, such as their intricate intracellular organization, can be traced back to a putative common ancestor that predated the broad diversity of extant eukaryotes. However, little is known about the nature and relative order of events that occurred in the path from preexisting prokaryotes to this already sophisticated ancestor. The origin of mitochondria from the endosymbiosis of an alphaproteobacterium is one of the few robustly established events to which most hypotheses on the origin of eukaryotes are anchored, but the debate is still open regarding the time of this acquisition, the nature of the host, and the ecological and metabolic interactions between the symbiotic partners. After the acquisition of mitochondria, eukaryotes underwent a fast radiation into several major clades whose phylogenetic relationships have been largely elusive. Recent progress in the comparative analyses of a growing number of genomes is shedding light on the early events of eukaryotic evolution as well as on the root and branching patterns of the tree of eukaryotes. Here I discuss current knowledge and debates on the origin and early evolution of eukaryotes. I focus particularly on how phylogenomic analyses have challenged some of the early assumptions about eukaryotic evolution, including the widespread idea that mitochondrial symbiosis in an archaeal host was the earliest event in eukaryogenesis.

RevDate: 2022-02-15
CmpDate: 2022-02-15

Makarov AA, Padilla-Mejia NE, MC Field (2021)

Evolution and diversification of the nuclear pore complex.

Biochemical Society transactions, 49(4):1601-1619.

The nuclear pore complex (NPC) is responsible for transport between the cytoplasm and nucleoplasm and one of the more intricate structures of eukaryotic cells. Typically composed of over 300 polypeptides, the NPC shares evolutionary origins with endo-membrane and intraflagellar transport system complexes. The modern NPC was fully established by the time of the last eukaryotic common ancestor and, hence, prior to eukaryote diversification. Despite the complexity, the NPC structure is surprisingly flexible with considerable variation between lineages. Here, we review diversification of the NPC in major taxa in view of recent advances in genomic and structural characterisation of plant, protist and nucleomorph NPCs and discuss the implications for NPC evolution. Furthermore, we highlight these changes in the context of mRNA export and consider how this process may have influenced NPC diversity. We reveal the NPC as a platform for continual evolution and adaptation.

RevDate: 2021-08-10
CmpDate: 2021-07-15

Anselmetti Y, El-Mabrouk N, Lafond M, et al (2021)

Gene tree and species tree reconciliation with endosymbiotic gene transfer.

Bioinformatics (Oxford, England), 37(Suppl_1):i120-i132.

MOTIVATION: It is largely established that all extant mitochondria originated from a unique endosymbiotic event integrating an α-proteobacterial genome into an eukaryotic cell. Subsequently, eukaryote evolution has been marked by episodes of gene transfer, mainly from the mitochondria to the nucleus, resulting in a significant reduction of the mitochondrial genome, eventually completely disappearing in some lineages. However, in other lineages such as in land plants, a high variability in gene repertoire distribution, including genes encoded in both the nuclear and mitochondrial genome, is an indication of an ongoing process of Endosymbiotic Gene Transfer (EGT). Understanding how both nuclear and mitochondrial genomes have been shaped by gene loss, duplication and transfer is expected to shed light on a number of open questions regarding the evolution of eukaryotes, including rooting of the eukaryotic tree.

RESULTS: We address the problem of inferring the evolution of a gene family through duplication, loss and EGT events, the latter considered as a special case of horizontal gene transfer occurring between the mitochondrial and nuclear genomes of the same species (in one direction or the other). We consider both EGT events resulting in maintaining (EGTcopy) or removing (EGTcut) the gene copy in the source genome. We present a linear-time algorithm for computing the DLE (Duplication, Loss and EGT) distance, as well as an optimal reconciled tree, for the unitary cost, and a dynamic programming algorithm allowing to output all optimal reconciliations for an arbitrary cost of operations. We illustrate the application of our EndoRex software and analyze different costs settings parameters on a plant dataset and discuss the resulting reconciled trees.

EndoRex implementation and supporting data are available on the GitHub repository via

RevDate: 2022-04-01
CmpDate: 2022-03-31

Vargová R, Wideman JG, Derelle R, et al (2021)

A Eukaryote-Wide Perspective on the Diversity and Evolution of the ARF GTPase Protein Family.

Genome biology and evolution, 13(8):.

The evolution of eukaryotic cellular complexity is interwoven with the extensive diversification of many protein families. One key family is the ARF GTPases that act in eukaryote-specific processes, including membrane traffic, tubulin assembly, actin dynamics, and cilia-related functions. Unfortunately, our understanding of the evolution of this family is limited. Sampling an extensive set of available genome and transcriptome sequences, we have assembled a data set of over 2,000 manually curated ARF family genes from 114 eukaryotic species, including many deeply diverged protist lineages, and carried out comprehensive molecular phylogenetic analyses. These reconstructed as many as 16 ARF family members present in the last eukaryotic common ancestor, nearly doubling the previously inferred ancient system complexity. Evidence for the wide occurrence and ancestral origin of Arf6, Arl13, and Arl16 is presented for the first time. Moreover, Arl17, Arl18, and SarB, newly described here, are absent from well-studied model organisms and as a result their function(s) remain unknown. Analyses of our data set revealed a previously unsuspected diversity of membrane association modes and domain architectures within the ARF family. We detail the step-wise expansion of the ARF family in the metazoan lineage, including discovery of several new animal-specific family members. Delving back to its earliest evolution in eukaryotes, the resolved relationship observed between the ARF family paralogs sets boundaries for scenarios of vesicle coat origins during eukaryogenesis. Altogether, our work fundamentally broadens the understanding of the diversity and evolution of a protein family underpinning the structural and functional complexity of the eukaryote cells.

RevDate: 2022-03-25
CmpDate: 2022-03-25

Devos DP (2021)

Reconciling Asgardarchaeota Phylogenetic Proximity to Eukaryotes and Planctomycetes Cellular Features in the Evolution of Life.

Molecular biology and evolution, 38(9):3531-3542.

The relationship between the three domains of life-Archaea, Bacteria, and Eukarya-is one of Biology's greatest mysteries. Current favored models imply two ancestral domains, Bacteria and Archaea, with eukaryotes originating within Archaea. This type of models has been supported by the recent description of the Asgardarchaeota, the closest prokaryotic relatives of eukaryotes. However, there are many problems associated with any scenarios implying that eukaryotes originated from within the Archaea, including genome mosaicism, phylogenies, the cellular organization of the Archaea, and their ancestral character. By contrast, all models of eukaryogenesis fail to consider two relevant discoveries: the detection of membrane coat proteins, and of phagocytosis-related processes in Planctomycetes, which are among the bacteria with the most developed endomembrane system. Consideration of these often overlooked features and others found in Planctomycetes and related bacteria suggest an evolutionary model based on a single ancestral domain. In this model, the proximity of Asgard and eukaryotes is not rejected but instead, Asgard are considered as diverging away from a common ancestor instead of on the way toward the eukaryotic ancestor. This model based on a single ancestral domain solves most of the ambiguities associated with the ones based on two ancestral domains. The single-domain model is better suited to explain the origin and evolution of all three domains of life, blurring the distinctions between them. Support for this model as well as the opportunities that it presents not only for reinterpreting previous results, but also for planning future experiments, are explored.

RevDate: 2021-08-11
CmpDate: 2021-08-11

Zhang S, Hama Y, N Mizushima (2021)

The evolution of autophagy proteins - diversification in eukaryotes and potential ancestors in prokaryotes.

Journal of cell science, 134(13):.

Autophagy is a degradative pathway for cytoplasmic constituents, and is conserved across eukaryotes. Autophagy-related (ATG) genes have undergone extensive multiplications and losses in different eukaryotic lineages, resulting in functional diversification and specialization. Notably, even though bacteria and archaea do not possess an autophagy pathway, they do harbor some remote homologs of Atg proteins, suggesting that preexisting proteins were recruited when the autophagy pathway developed during eukaryogenesis. In this Review, we summarize our current knowledge on the distribution of Atg proteins within eukaryotes and outline the major multiplication and loss events within the eukaryotic tree. We also discuss the potential prokaryotic homologs of Atg proteins identified to date, emphasizing the evolutionary relationships and functional differences between prokaryotic and eukaryotic proteins.

RevDate: 2021-07-04

Tan DX (2021)

Genesis of the nucleus from bacterial sporulation: A simple hypothesis of eukaryotic origin.

Neuro endocrinology letters, 42(2):113-127 pii:NEL420221R01 [Epub ahead of print].

The most complexed issue of eukaryogenesis is the origin of the nucleus. Many hypotheses have been forwarded to explain this. Most of them are complicated and intangible. Here, a new and relatively simple hypothesis to address this unresolved problem has been hypothesized. This hypothesis is denominated as "Theory of Nucleus Origin from Bacterial Sporulation" (TNOBS). The hypothesis points out that the nucleus may be derived from a bacterial endospore, particularly, when sporulation is arrested at stage 4 due to a gene mutation. At this stage, a double membrane structure containing a chromosome (foreospore) has developed, which is reminiscent of a nucleus. In addition to the forespore, the mother cell also contains an additional chromosome. This morphologically specific cell is referred as a proto-nucleate cell (PTC). The PTC requires additional energy to maintain their newly formed endomembrane compartment (protonucleus). This energy demand has the potential of driving the expression of genes for energy production from the cytosolic chromosome which finally evolves to mitochondria, whereas the forespore develops to the nucleus. This TNOBS considers the nucleus and mitochondrion having derived simultaneously in the same cell. Moreover, this scenario avoids the difficulty to explain how an α-proteobacterium (precursor of mitochondria) can be taken up by the host despite of lacking capacity for classic endocytosis. It is further suggested that PTC generation may not be an extremely rare event in nature due to the widely existing spore-forming bacteria and frequent mutations. TNOBS is comparably simple and may, in some of its principle traits, be even reproducible under laboratory conditions.

RevDate: 2021-09-21
CmpDate: 2021-09-21

Almojil D, Bourgeois Y, Falis M, et al (2021)

The Structural, Functional and Evolutionary Impact of Transposable Elements in Eukaryotes.

Genes, 12(6):.

Transposable elements (TEs) are nearly ubiquitous in eukaryotes. The increase in genomic data, as well as progress in genome annotation and molecular biology techniques, have revealed the vast number of ways mobile elements have impacted the evolution of eukaryotes. In addition to being the main cause of difference in haploid genome size, TEs have affected the overall organization of genomes by accumulating preferentially in some genomic regions, by causing structural rearrangements or by modifying the recombination rate. Although the vast majority of insertions is neutral or deleterious, TEs have been an important source of evolutionary novelties and have played a determinant role in the evolution of fundamental biological processes. TEs have been recruited in the regulation of host genes and are implicated in the evolution of regulatory networks. They have also served as a source of protein-coding sequences or even entire genes. The impact of TEs on eukaryotic evolution is only now being fully appreciated and the role they may play in a number of biological processes, such as speciation and adaptation, remains to be deciphered.


ESP Quick Facts

ESP Origins

In the early 1990's, Robert Robbins was a faculty member at Johns Hopkins, where he directed the informatics core of GDB — the human gene-mapping database of the international human genome project. To share papers with colleagues around the world, he set up a small paper-sharing section on his personal web page. This small project evolved into The Electronic Scholarly Publishing Project.

ESP Support

In 1995, Robbins became the VP/IT of the Fred Hutchinson Cancer Research Center in Seattle, WA. Soon after arriving in Seattle, Robbins secured funding, through the ELSI component of the US Human Genome Project, to create the original ESP.ORG web site, with the formal goal of providing free, world-wide access to the literature of classical genetics.

ESP Rationale

Although the methods of molecular biology can seem almost magical to the uninitiated, the original techniques of classical genetics are readily appreciated by one and all: cross individuals that differ in some inherited trait, collect all of the progeny, score their attributes, and propose mechanisms to explain the patterns of inheritance observed.

ESP Goal

In reading the early works of classical genetics, one is drawn, almost inexorably, into ever more complex models, until molecular explanations begin to seem both necessary and natural. At that point, the tools for understanding genome research are at hand. Assisting readers reach this point was the original goal of The Electronic Scholarly Publishing Project.

ESP Usage

Usage of the site grew rapidly and has remained high. Faculty began to use the site for their assigned readings. Other on-line publishers, ranging from The New York Times to Nature referenced ESP materials in their own publications. Nobel laureates (e.g., Joshua Lederberg) regularly used the site and even wrote to suggest changes and improvements.

ESP Content

When the site began, no journals were making their early content available in digital format. As a result, ESP was obliged to digitize classic literature before it could be made available. For many important papers — such as Mendel's original paper or the first genetic map — ESP had to produce entirely new typeset versions of the works, if they were to be available in a high-quality format.

ESP Help

Early support from the DOE component of the Human Genome Project was critically important for getting the ESP project on a firm foundation. Since that funding ended (nearly 20 years ago), the project has been operated as a purely volunteer effort. Anyone wishing to assist in these efforts should send an email to Robbins.

ESP Plans

With the development of methods for adding typeset side notes to PDF files, the ESP project now plans to add annotated versions of some classical papers to its holdings. We also plan to add new reference and pedagogical material. We have already started providing regularly updated, comprehensive bibliographies to the ESP.ORG site.

Electronic Scholarly Publishing
961 Red Tail Lane
Bellingham, WA 98226

E-mail: RJR8222 @

Papers in Classical Genetics

The ESP began as an effort to share a handful of key papers from the early days of classical genetics. Now the collection has grown to include hundreds of papers, in full-text format.

Digital Books

Along with papers on classical genetics, ESP offers a collection of full-text digital books, including many works by Darwin (and even a collection of poetry — Chicago Poems by Carl Sandburg).


ESP now offers a much improved and expanded collection of timelines, designed to give the user choice over subject matter and dates.


Biographical information about many key scientists.

Selected Bibliographies

Bibliographies on several topics of potential interest to the ESP community are now being automatically maintained and generated on the ESP site.

ESP Picks from Around the Web (updated 07 JUL 2018 )