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

Nobs, Stephanie-Jane; MacLeod, Fraser; Wong, Hon Lun; Burns, Brendan P.

doi:10.1016/j.tim.2021.11.003

Cited by 9 publications

(11 citation statements)

References 81 publications

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“…We propose that the absence of Hel308-Ski2 in single genomes scattered throughout the archaea taxonomy results from independent loss events, except in Asgard where this may be due to the incompleteness of their genome. Eukaryotic PolQ/HelQ DNA helicases have been found to branch with the Hel308-Ski2 Asgard sequences (Figure 1B ), consistent with the hypothesis that eukaryal domain emerged from Asgard archaea ( 1 , 2 ). Previous work assigned the function of archaeal Hel308 members to DNA metabolism ( 32 , 35 , 36 ).…”

Section: Discussionsupporting

confidence: 83%

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Evolutionary and functional insights into the Ski2-like helicase family in Archaea: a comparison of Thermococcales ASH-Ski2 and Hel308 activities

Batista,

Langendijk-Genevaux,

Kwapisz

et al. 2024

NAR Genomics and Bioinformatics

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RNA helicases perform essential housekeeping and regulatory functions in all domains of life by binding and unwinding RNA molecules. The Ski2-like proteins are primordial helicases that play an active role in eukaryotic RNA homeostasis pathways, with multiple homologs having specialized functions. The significance of the expansion and diversity of Ski2-like proteins in Archaea, the third domain of life, has not yet been established. Here, by studying the phylogenetic diversity of Ski2-like helicases among archaeal genomes and the enzymatic activities of those in Thermococcales, we provide further evidence of the function of this protein family in archaeal metabolism of nucleic acids. We show that, in the course of evolution, ASH-Ski2 and Hel308-Ski2, the two main groups of Ski2-like proteins, have diverged in their biological functions. Whereas Hel308 has been shown to mainly act on DNA, we show that ASH-Ski2, previously described to be associated with the 5′-3′ aRNase J exonuclease, acts on RNA by supporting an efficient annealing activity, but also an RNA unwinding with a 3′-5′ polarity. To gain insights into the function of Ski2, we also analyse the transcriptome of Thermococcus barophilus ΔASH-Ski2 mutant strain and provide evidence of the importance of ASH-Ski2 in cellular metabolism pathways related to translation.

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Section: Discussionsupporting

confidence: 83%

“…Archaea are critical research models for gaining insights into the origin of the eukaryotic cell and the evolution of life, as well as for studying biogeochemical processes ( 1 , 2 , 3 ). A recent evolutionary scenario proposes that the eukaryal domain originated within the archaeal domain, arising from the Asgard archaea ( 4 ).…”

Section: Introductionmentioning

confidence: 99%

Evolutionary and functional insights into the Ski2-like helicase family in Archaea: a comparison of Thermococcales ASH-Ski2 and Hel308 activities

Batista,

Langendijk-Genevaux,

Kwapisz

et al. 2024

NAR Genomics and Bioinformatics

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“…In conclusion, our comparatively fast-growing lokiarchaeal culture enabled us to study its cell architecture in a near-native state. We discovered an elaborate actin-based cytoskeleton in Asgard archaea, which has long been hypothesized [4][5][6][42][43][44] , but has not been visualized. The cytoskeleton is probably a hallmark structure of all Asgard archaea, as Lokiactin is conserved in genomes of all Asgardarchaeota classes.…”

Section: Discussionmentioning

confidence: 95%

Section: Discussionmentioning

confidence: 95%

“…Their genomes contain hundreds of eukaryotic signature proteins (ESPs), which inspired hypotheses on the evolution of the eukaryotic cell [1][2][3] . A role of ESPs in the formation of an elaborate cytoskeleton and complex cellular structures has been postulated [4][5][6] , but never visualized. Here we describe a highly enriched culture of 'Candidatus Lokiarchaeum ossiferum', a member of the Asgard phylum, which thrives anaerobically at 20 °C on organic carbon sources.…”

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confidence: 99%

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Actin cytoskeleton and complex cell architecture in an Asgard archaeon

Rodrigues-Oliveira

Wollweber

Ponce‐Toledo

et al. 2022

Nature

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Asgard archaea are considered to be the closest known relatives of eukaryotes. Their genomes contain hundreds of eukaryotic signature proteins (ESPs), which inspired hypotheses on the evolution of the eukaryotic cell1–3. A role of ESPs in the formation of an elaborate cytoskeleton and complex cellular structures has been postulated4–6, but never visualized. Here we describe a highly enriched culture of ‘Candidatus Lokiarchaeum ossiferum’, a member of the Asgard phylum, which thrives anaerobically at 20 °C on organic carbon sources. It divides every 7–14 days, reaches cell densities of up to 5 × 107 cells per ml and has a significantly larger genome compared with the single previously cultivated Asgard strain7. ESPs represent 5% of its protein-coding genes, including four actin homologues. We imaged the enrichment culture using cryo-electron tomography, identifying ‘Ca. L. ossiferum’ cells on the basis of characteristic expansion segments of their ribosomes. Cells exhibited coccoid cell bodies and a network of branched protrusions with frequent constrictions. The cell envelope consists of a single membrane and complex surface structures. A long-range cytoskeleton extends throughout the cell bodies, protrusions and constrictions. The twisted double-stranded architecture of the filaments is consistent with F-actin. Immunostaining indicates that the filaments comprise Lokiactin—one of the most highly conserved ESPs in Asgard archaea. We propose that a complex actin-based cytoskeleton predated the emergence of the first eukaryotes and was a crucial feature in the evolution of the Asgard phylum by scaffolding elaborate cellular structures.

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Carl Woese: Still ahead of our time

Forterre

2022

mLife

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

Cited by 9 publications

References 81 publications

Evolutionary and functional insights into the Ski2-like helicase family in Archaea: a comparison of Thermococcales ASH-Ski2 and Hel308 activities

Evolutionary and functional insights into the Ski2-like helicase family in Archaea: a comparison of Thermococcales ASH-Ski2 and Hel308 activities

Actin cytoskeleton and complex cell architecture in an Asgard archaeon

Carl Woese: Still ahead of our time

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