From archaeon to eukaryote: the evolutionary dark ages of the eukaryotic cell

2013 ◽  
Vol 41 (1) ◽  
pp. 451-457 ◽  
Author(s):  
Joran Martijn ◽  
Thijs J.G. Ettema
Keyword(s):  
Eukaryotic Cell ◽  
Convincing Evidence ◽  
Evolutionary Transition ◽  
Fusion Event ◽  
Genomic Features ◽  
Archaeal Lineage ◽  
Complex Features ◽  
Cellular Fusion ◽  
Origin Of Eukaryotes ◽  
Archaeal Ancestor

The evolutionary origin of the eukaryotic cell represents an enigmatic, yet largely incomplete, puzzle. Several mutually incompatible scenarios have been proposed to explain how the eukaryotic domain of life could have emerged. To date, convincing evidence for these scenarios in the form of intermediate stages of the proposed eukaryogenesis trajectories is lacking, presenting the emergence of the complex features of the eukaryotic cell as an evolutionary deus ex machina. However, recent advances in the field of phylogenomics have started to lend support for a model that places a cellular fusion event at the basis of the origin of eukaryotes (symbiogenesis), involving the merger of an as yet unknown archaeal lineage that most probably belongs to the recently proposed ‘TACK superphylum’ (comprising Thaumarchaeota, Aigarchaeota, Crenarchaeota and Korarchaeota) with an alphaproteobacterium (the protomitochondrion). Interestingly, an increasing number of so-called ESPs (eukaryotic signature proteins) is being discovered in recently sequenced archaeal genomes, indicating that the archaeal ancestor of the eukaryotic cell might have been more eukaryotic in nature than presumed previously, and might, for example, have comprised primitive phagocytotic capabilities. In the present paper, we review the evolutionary transition from archaeon to eukaryote, and propose a new model for the emergence of the eukaryotic cell, the ‘PhAT (phagocytosing archaeon theory)’, which explains the emergence of the cellular and genomic features of eukaryotes in the light of a transiently complex phagocytosing archaeon.

scholarly journals Isolation of an archaeon at the prokaryote–eukaryote interface

Nature ◽  
2020 ◽  
Vol 577 (7791) ◽  
pp. 519-525 ◽  
Author(s):  
Hiroyuki Imachi ◽  
Masaru K. Nobu ◽  
Nozomi Nakahara ◽  
Yuki Morono ◽  
Miyuki Ogawara ◽  
...  
Keyword(s):  
Amino Acids ◽  
Marine Sediment ◽  
Current Data ◽  
Evolutionary Transition ◽  
Hypothetical Model ◽  
Genomic Features ◽  
Archaeal Lineage ◽  
Slow Growing ◽  
Origin Of Eukaryotes

Abstract The origin of eukaryotes remains unclear1–4. Current data suggest that eukaryotes may have emerged from an archaeal lineage known as ‘Asgard’ archaea5,6. Despite the eukaryote-like genomic features that are found in these archaea, the evolutionary transition from archaea to eukaryotes remains unclear, owing to the lack of cultured representatives and corresponding physiological insights. Here we report the decade-long isolation of an Asgard archaeon related to Lokiarchaeota from deep marine sediment. The archaeon—‘Candidatus Prometheoarchaeum syntrophicum’ strain MK-D1—is an anaerobic, extremely slow-growing, small coccus (around 550 nm in diameter) that degrades amino acids through syntrophy. Although eukaryote-like intracellular complexes have been proposed for Asgard archaea6, the isolate has no visible organelle-like structure. Instead, Ca. P. syntrophicum is morphologically complex and has unique protrusions that are long and often branching. On the basis of the available data obtained from cultivation and genomics, and reasoned interpretations of the existing literature, we propose a hypothetical model for eukaryogenesis, termed the entangle–engulf–endogenize (also known as E3) model.

scholarly journals Isolation of an archaeon at the prokaryote-eukaryote interface

2019 ◽  
Author(s):  
Hiroyuki Imachi ◽  
Masaru K. Nobu ◽  
Nozomi Nakahara ◽  
Yuki Morono ◽  
Miyuki Ogawara ◽  
...  
Keyword(s):  
Amino Acids ◽  
Marine Sediment ◽  
Current Data ◽  
Evolutionary Transition ◽  
Genomic Features ◽  
Morphological Complexity ◽  
Archaeal Lineage ◽  
Slow Growing ◽  
Origin Of Eukaryotes

AbstractThe origin of eukaryotes remains enigmatic. Current data suggests that eukaryotes may have risen from an archaeal lineage known as “Asgard archaea”. Despite the eukaryote-like genomic features found in these archaea, the evolutionary transition from archaea to eukaryotes remains unclear due to the lack of cultured representatives and corresponding physiological insight. Here we report the decade-long isolation of a Lokiarchaeota-related Asgard archaeon from deep marine sediment. The archaeon, “Candidatus Prometheoarchaeum syntrophicum strain MK-D1”, is an anaerobic, extremely slow-growing, small cocci (∼550 nm), that degrades amino acids through syntrophy. Although eukaryote-like intracellular complexities have been proposed for Asgard archaea, the isolate has no visible organella-like structure. Ca. P. syntrophicum instead displays morphological complexity – unique long, and often, branching protrusions. Based on cultivation and genomics, we propose an “Entangle-Engulf-Enslave (E3) model” for eukaryogenesis through archaea-alphaproteobacteria symbiosis mediated by the physical complexities and metabolic dependency of the hosting archaeon.

Origin and Early Evolution of the Eukaryotic Cell

2021 ◽  
Vol 75 (1) ◽  
Author(s):  
Toni Gabaldón
Keyword(s):  
Current Knowledge ◽  
Eukaryotic Cell ◽  
Early Evolution ◽  
Annual Review ◽  
Publication Date ◽  
Eukaryotic Evolution ◽  
Life Itself ◽  
Metabolic Interactions ◽  
Phylogenomic Analyses ◽  
Origin Of Eukaryotes

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. Expected final online publication date for the Annual Review of Microbiology, Volume 75 is October 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

The comparative biochemistry of viruses and humans: an evolutionary path towards autoimmunity

2019 ◽  
Vol 400 (5) ◽  
pp. 629-638 ◽  
Author(s):  
Darja Kanduc
Keyword(s):  
Measles Virus ◽  
Influenza A ◽  
Viral Infections ◽  
Sequence Similarity ◽  
Eukaryotic Cell ◽  
Point Of View ◽  
Peptide Sequence ◽  
Human Viruses ◽  
Archaeal Ancestor ◽  
Borna Disease

Abstract Analyses of the peptide sharing between five common human viruses (Borna disease virus, influenza A virus, measles virus, mumps virus and rubella virus) and the human proteome highlight a massive viral vs. human peptide overlap that is mathematically unexpected. Evolutionarily, the data underscore a strict relationship between viruses and the origin of eukaryotic cells. Indeed, according to the viral eukaryogenesis hypothesis and in light of the endosymbiotic theory, the first eukaryotic cell (our lineage) originated as a consortium consisting of an archaeal ancestor of the eukaryotic cytoplasm, a bacterial ancestor of the mitochondria and a viral ancestor of the nucleus. From a pathologic point of view, the peptide sequence similarity between viruses and humans may provide a molecular platform for autoimmune crossreactions during immune responses following viral infections/immunizations.

scholarly journals Conflict and cooperation in eukaryogenesis: implications for the timing of endosymbiosis and the evolution of sex

2015 ◽  
Author(s):  
Arunas L Radzvilavicius ◽  
Neil W Blackstone
Keyword(s):  
Cell Fusion ◽  
Mitochondrial Gene ◽  
Evolutionary Process ◽  
Eukaryotic Cell ◽  
Evolutionary Transition ◽  
Evolutionary Transitions ◽  
Conflict And Cooperation ◽  
Conflict Mediation ◽  
Considerable Debate ◽  
History Of

The complex eukaryotic cell is a result of an ancient endosymbiosis and one of the major evolutionary transitions. The timing of key eukaryotic innovations relative to the acquisition of mitochondria remains subject to considerable debate, yet the evolutionary process itself might constrain the order of these events. Endosymbiosis entailed levels-of-selection conflicts, and mechanisms of conflict mediation had to evolve for eukaryogenesis to proceed. The initial mechanisms of conflict mediation were based on the pathways inherited from prokaryotic symbionts and led to metabolic homeostasis in the eukaryotic cell, while later mechanisms (e.g., mitochondrial gene transfer) contributed to the expansion of the eukaryotic genome. Perhaps the greatest opportunity for conflict arose with the emergence of sex involving whole-cell fusion. While early evolution of cell fusion may have affected symbiont acquisition, sex together with the competitive symbiont behaviour would have destabilised the emerging higher-level unit. Cytoplasmic mixing, on the other hand, would have been beneficial for selfish endosymbionts, capable of using their own metabolism to manipulate the life history of the host. Given the results of our mathematical modelling, we argue that sex represents a rather late proto- eukaryotic innovation, allowing for the growth of the chimeric nucleus and contributing to the successful completion of the evolutionary transition.

scholarly journals Exploring microbial dark matter to resolve the deep archaeal ancestry of eukaryotes

2015 ◽  
Vol 370 (1678) ◽  
pp. 20140328 ◽  
Author(s):  
Jimmy H. Saw ◽  
Anja Spang ◽  
Katarzyna Zaremba-Niedzwiedzka ◽  
Lina Juzokaite ◽  
Jeremy A. Dodsworth ◽  
...  
Keyword(s):  
Dark Matter ◽  
Host Cell ◽  
Draft Genome ◽  
Eukaryotic Cell ◽  
Microbial Evolution ◽  
Current View ◽  
Sequencing Technologies ◽  
Evolution Of Life ◽  
Origin Of Eukaryotes ◽  
Generation Sequencing

The origin of eukaryotes represents an enigmatic puzzle, which is still lacking a number of essential pieces. Whereas it is currently accepted that the process of eukaryogenesis involved an interplay between a host cell and an alphaproteobacterial endosymbiont, we currently lack detailed information regarding the identity and nature of these players. A number of studies have provided increasing support for the emergence of the eukaryotic host cell from within the archaeal domain of life, displaying a specific affiliation with the archaeal TACK superphylum. Recent studies have shown that genomic exploration of yet-uncultivated archaea, the so-called archaeal ‘dark matter’, is able to provide unprecedented insights into the process of eukaryogenesis. Here, we provide an overview of state-of-the-art cultivation-independent approaches, and demonstrate how these methods were used to obtain draft genome sequences of several novel members of the TACK superphylum, including Lokiarchaeum, two representatives of the Miscellaneous Crenarchaeotal Group (Bathyarchaeota), and a Korarchaeum -related lineage. The maturation of cultivation-independent genomics approaches, as well as future developments in next-generation sequencing technologies, will revolutionize our current view of microbial evolution and diversity, and provide profound new insights into the early evolution of life, including the enigmatic origin of the eukaryotic cell.

scholarly journals Eukaryogenesis, how special really?

2015 ◽  
Vol 112 (33) ◽  
pp. 10278-10285 ◽  
Author(s):  
Austin Booth ◽  
W. Ford Doolittle
Keyword(s):  
Eukaryotic Cell ◽  
Evolutionary Transition ◽  
Evolutionary Potential ◽  
Evolutionary Transitions ◽  
History Of Research ◽  
Evolution Of Life ◽  
Widespread Acceptance ◽  
Statistical Support ◽  
History Of ◽  
Rhetorical Value

Eukaryogenesis is widely viewed as an improbable evolutionary transition uniquely affecting the evolution of life on this planet. However, scientific and popular rhetoric extolling this event as a singularity lacks rigorous evidential and statistical support. Here, we question several of the usual claims about the specialness of eukaryogenesis, focusing on both eukaryogenesis as a process and its outcome, the eukaryotic cell. We argue in favor of four ideas. First, the criteria by which we judge eukaryogenesis to have required a genuinely unlikely series of events 2 billion years in the making are being eroded by discoveries that fill in the gaps of the prokaryote:eukaryote “discontinuity.” Second, eukaryogenesis confronts evolutionary theory in ways not different from other evolutionary transitions in individuality; parallel systems can be found at several hierarchical levels. Third, identifying which of several complex cellular features confer on eukaryotes a putative richer evolutionary potential remains an area of speculation: various keys to success have been proposed and rejected over the five-decade history of research in this area. Fourth, and perhaps most importantly, it is difficult and may be impossible to eliminate eukaryocentric bias from the measures by which eukaryotes as a whole are judged to have achieved greater success than prokaryotes as a whole. Overall, we question whether premises of existing theories about the uniqueness of eukaryogenesis and the greater evolutionary potential of eukaryotes have been objectively formulated and whether, despite widespread acceptance that eukaryogenesis was “special,” any such notion has more than rhetorical value.

scholarly journals The Common Ancestor of Archaea and Eukarya Was Not an Archaeon

Archaea ◽  
2013 ◽  
Vol 2013 ◽  
pp. 1-18 ◽  
Author(s):  
Patrick Forterre
Keyword(s):  
Common Ancestor ◽  
Phylogenetic Analyses ◽  
Critical Role ◽  
Last Common Ancestor ◽  
Dna Viruses ◽  
The Common ◽  
Basic Features ◽  
Origin Of Eukaryotes ◽  
Archaeal Ancestor ◽  
Selection Of

It is often assumed that eukarya originated from archaea. This view has been recently supported by phylogenetic analyses in which eukarya are nested within archaea. Here, I argue that these analyses are not reliable, and I critically discuss archaeal ancestor scenarios, as well as fusion scenarios for the origin of eukaryotes. Based on recognized evolutionary trends toward reduction in archaea and toward complexity in eukarya, I suggest that their last common ancestor was more complex than modern archaea but simpler than modern eukaryotes (the bug in-between scenario). I propose that the ancestors of archaea (and bacteria) escaped protoeukaryotic predators by invading high temperature biotopes, triggering their reductive evolution toward the “prokaryotic” phenotype (the thermoreduction hypothesis). Intriguingly, whereas archaea and eukarya share many basic features at the molecular level, the archaeal mobilome resembles more the bacterial than the eukaryotic one. I suggest that selection of different parts of the ancestral virosphere at the onset of the three domains played a critical role in shaping their respective biology. Eukarya probably evolved toward complexity with the help of retroviruses and large DNA viruses, whereas similar selection pressure (thermoreduction) could explain why the archaeal and bacterial mobilomes somehow resemble each other.

scholarly journals Reproduction, symbiosis, and the eukaryotic cell

2015 ◽  
Vol 112 (33) ◽  
pp. 10120-10125 ◽  
Author(s):  
Peter Godfrey-Smith
Keyword(s):  
Conceptual Framework ◽  
Eukaryotic Cell ◽  
Evolutionary Sequence ◽  
Evolutionary Transition ◽  
Units Of Selection ◽  
Symbiotic Associations

This paper develops a conceptual framework for addressing questions about reproduction, individuality, and the units of selection in symbiotic associations, with special attention to the origin of the eukaryotic cell. Three kinds of reproduction are distinguished, and a possible evolutionary sequence giving rise to a mitochondrion-containing eukaryotic cell from an endosymbiotic partnership is analyzed as a series of transitions between each of the three forms of reproduction. The sequence of changes seen in this “egalitarian” evolutionary transition is compared with those that apply in “fraternal” transitions, such as the evolution of multicellularity in animals.

scholarly journals Arguments Reinforcing the Three-Domain View of Diversified Cellular Life

Archaea ◽  
2016 ◽  
Vol 2016 ◽  
pp. 1-11 ◽  
Author(s):  
Arshan Nasir ◽  
Kyung Mo Kim ◽  
Violette Da Cunha ◽  
Gustavo Caetano-Anollés
Keyword(s):  
Cell Movement ◽  
Protein Domain ◽  
Bacterial Cells ◽  
Domain Structures ◽  
Cellular Life ◽  
Protein Domain Structure ◽  
Gain Loss ◽  
Cellular Compartments ◽  
Origin Of Eukaryotes ◽  
Archaeal Ancestor

The archaeal ancestor scenario (AAS) for the origin of eukaryotes implies the emergence of a new kind of organism from the fusion of ancestral archaeal and bacterial cells. Equipped with this “chimeric” molecular arsenal, the resulting cell would gradually accumulate unique genes and develop the complex molecular machineries and cellular compartments that are hallmarks of modern eukaryotes. In this regard, proteins related to phagocytosis and cell movement should be present in the archaeal ancestor, thus identifying the recently described candidate archaeal phylum “Lokiarchaeota” as resembling a possible candidate ancestor of eukaryotes. Despite its appeal, AAS seems incompatible with the genomic, molecular, and biochemical differences that exist between Archaea and Eukarya. In particular, the distribution of conserved protein domain structures in the proteomes of cellular organisms and viruses appears hard to reconcile with the AAS. In addition, concerns related to taxon and character sampling, presupposing bacterial outgroups in phylogenies, and nonuniform effects of protein domain structure rearrangement and gain/loss in concatenated alignments of protein sequences cast further doubt on AAS-supporting phylogenies. Here, we evaluate AAS against the traditional “three-domain” world of cellular organisms and propose that the discovery of Lokiarchaeota could be better reconciled under the latter view, especially in light of several additional biological and technical considerations.

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