Genomes of Asgard archaea encode profilins that regulate actin

Akıl, Caner; Robinson, Robert

doi:10.1038/s41586-018-0548-6

Cited by 108 publications

(167 citation statements)

References 29 publications

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“…The functional classes of genes that were created during this transition from FECA to LECA primarily appear to have prokaryote origins, which lends additional credence to an increasing trend in the literature. There's been a plethora of research in recent years on prokaryote encroachment into many aspects of biology that have been traditionally considered eukaryote-specific [6][7][8]39,[74][75][76] , it is perhaps worth examining the basis for the competing theories of eukaryogenesis. The apparent conflict between mito-late and mito-early theories hinges on our understanding of the complexity of prokaryotes.…”

Section: Discussionmentioning

confidence: 99%

“…Many proteins that until recently were thought to be eukaryote-specific now seem to have homologs in these Asgard genomes. Specifically, components of the ESCRT system, the TRAPP membrane-trafficking systems, the ubiquitin modifier system, the actin cytoskeleton, and an expanded range of GTPases have been found in the metagenomic assembles that identified the Asgardarchaeota species [6][7][8] . Increasingly characteristic structures and biology previously used to characterize eukaryotes appear to have its origins from within this archaeal group.…”

Section: Introductionmentioning

confidence: 99%

“…This evidence was later found to be a phylogenetic artefact, and mitochrondrially derived genes are present in the nuclear genomes of the supposed amitochondriate archezoa species 38 . But with the increasing body of literature on the surprising eukaryote-like properties of the Asgard Archaea [5][6][7]8 , it increasingly appears that prokaryote complexity has been consistently underestimated. For example, while members of the Planctomycetes, Verrucomicrobiae, and Chlamydiae (PVC) bacterial Superphylum don't have true compartmentalized nor nucleated cells they demonstrate a striking level of intracellular structural complexity and there are other examples of true membrane-bound vesicles in prokaryotes 39,40 .…”

Section: Introductionmentioning

confidence: 99%

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Reconstructing and Analysing The Genome of The Last Eukaryote Common Ancestor to Better Understand the Transition from FECA to LECA

Newman

Moore

et al. 2019

Preprint

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It is still a matter of debate whether the First Eukaryote Common Ancestor (FECA) arose from the merger of an archaeal host with an alphaproteobacterium, or was a proto-eukaryote with significant eukaryotic characteristics way before endosymbiosis occurred. The Last Eukaryote Common Ancestor (LECA) as its descendant is thought to be an entity that possessed functional and cellular complexity comparable to modern organisms. The precise nature and physiology of both of these organisms has been a long-standing, unanswered question in evolutionary and cell biology. Recently, a much broader diversity of eukaryotic genomes has become available and this means we can reconstruct early eukaryote evolution with a greater deal of precision. Here, we reconstruct a hypothetical genome for LECA from modern eukaryote genomes. The constituent genes were mapped onto 454 pathways from the KEGG database covering cellular, genetic, and metabolic processes across six model species to provide functional insights into it's capabilities. We reconstruct a LECA that was a facultatively anaerobic, single-celled organism, similar to a modern Protist possessing complex predatory and sexual behaviour. We go on to examine how much of these capabilities arose along the FECA-to-LECA transition period. We see a at least 1,554 genes gained by FECA during this evolutionary period with extensive remodelling of pathways relating to lipid metabolism, cellular processes, genetic information processing, protein processing, and signalling. We extracted the BRITE classifications for the genes from the KEGG database, which arose during the transition from FECA-to-LECA and examine the types of genes that saw the most gains and what novel classifications were introduced. Two-thirds of our reconstructed LECA genome appears to be prokaryote in origin and the remaining third consists of genes with functional classifications that originate from prokaryote homologs in our LECA genome. Signal transduction and Post Translational Modification elements stand out as the primary novel classes of genes developed during this period. These results suggest that largely the eukaryote common ancestors achieved the defining characteristics of modern eukaryotes by primarily expanding on prokaryote biology and gene families.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Reconstructing and Analysing The Genome of The Last Eukaryote Common Ancestor to Better Understand the Transition from FECA to LECA

Newman

Moore

et al. 2019

Preprint

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“…Gene sequences were synthesized and codon optimized for E. coli (GenScript) and placed in the pSY5 vector 3,26 . Proteins were expressed as described previously 3 NaCl, 1 mM TCEP and 1mM EGTA) were performed as described previously 3 . Asgard gelsolin fractions were pooled and concentrated (10000 MWCO Vivaspin concentrator, Vivascience).…”

Section: Protein Expression and Purificationmentioning

confidence: 99%

Complex eukaryotic-like actin regulation systems from Asgard archaea

Akıl

Tran

Orhant‐Prioux

et al. 2019

Preprint

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Asgard archaea genomes contain potential eukaryotic-like genes that provide intriguing insight for the evolution of eukaryotes. The actin polymerization/depolymerization cycle is critical for providing force and structure for a variety of processes in eukaryotes, including membrane remodelling. Here, we identify actin filament severing, capping, annealing and bundling, and monomer sequestration activities by gelsolin proteins from Thorarchaeota (Thor), which complete a eukaryote-like actin depolymerization cycle. Thor gelsolins are comprised of one or two copies of the prototypical gelsolin domain and appear to be a record of an initial pre-eukaryotic gene duplication event, since eukaryotic gelsolins are generally comprised of three to six domains. X-ray crystal structure determination of these proteins in complex with mammalian actin revealed similar interactions to the first domain of human gelsolin. Asgard two-domain, but not one-domain, gelsolins contain calcium-binding sites, which is manifested in calciumcontrolled activities. Expression of two-domain gelsolins in mammalian cells led to enhanced actin filament disassembly on ionomycin-triggered calcium release. This functional demonstration, at the cellular level, provides evidence for calcium-regulated actin cytoskeleton in Asgard archaea, and indicates that the calcium-regulated actin cytoskeleton predates eukaryotes. In eukaryotes, dynamic bundled filaments are responsible for shaping filopodia and microvilli. By correlation, the formation of the protrusions observed from Lokiarchaeota cell bodies may involve gelsolin-regulated actin structures.

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“…A dynamic cytoskeleton and trafficking system, perhaps enabling primitive phagocytosis 24 , might have been essential for the host to take up the bacterial symbiont. Molecular and cell biology research in these archaea, from which the first results have recently become public 25,26 , is highly promising to obtain more insight into the nature of the host lineage. In addition to a reconstruction of the host, further exploration of the numerous acquisitions, inventions and duplications during eukaryogenesis is key to fully unravelling the origin of eukaryotes.…”

Section: Main Textmentioning

confidence: 99%

Timing the origin of eukaryotic cellular complexity with ancient duplications

Vosseberg

Hooff

Marcet‐Houben

et al. 2019

Preprint

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Eukaryogenesis is one of the most enigmatic evolutionary transitions, during which simple prokaryotic cells gave rise to complex eukaryotic cells 1,2 . The last eukaryotic common ancestor (LECA) harboured intracellular compartments, including mitochondria. In addition to mitochondrial endosymbiosis, eukaryogenesis was driven by numerous gene acquisitions 3 , inventions and duplications 4 , which shaped the ancestral eukaryotic traits. While evolutionary intermediates are lacking, gene duplications allow us to elucidate the order of events by which eukaryotes originated. Here we reconstruct successive steps during eukaryogenesis using phylogenomics and show that mitochondrial endosymbiosis was an intermediate episode. We found that gene duplications roughly doubled the proto-eukaryotic genome, with families inherited from the Asgard archaea-related host being duplicated most. Importantly, by relatively timing events using branch lengths we inferred that duplications of archaeal families occurred throughout eukaryogenesis, both before and after the acquisition of bacterial genes. Duplications in cytoskeletal and membrane trafficking families were among the earliest events, whereas most other families expanded primarily after mitochondrial endosymbiosis. Altogether, we demonstrate that the host that engulfed the protomitochondrion had some eukaryote-like complexity, which further increased drastically upon mitochondrial acquisition. This scenario bridges the signs of complexity observed in Asgard archaeal genomes 5,6 to the proposed role of mitochondria in triggering eukaryogenesis 7,8 .

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Genomes of Asgard archaea encode profilins that regulate actin

Cited by 108 publications

References 29 publications

Reconstructing and Analysing The Genome of The Last Eukaryote Common Ancestor to Better Understand the Transition from FECA to LECA

Reconstructing and Analysing The Genome of The Last Eukaryote Common Ancestor to Better Understand the Transition from FECA to LECA

Complex eukaryotic-like actin regulation systems from Asgard archaea

Timing the origin of eukaryotic cellular complexity with ancient duplications

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