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Evolution of diverse cell division and vesicle formation systems in Archaea

Nature Reviews Microbiology volume 8, pages 731–741 (2010)Cite this article

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Key Points

  • Recently, the unexpected discovery was made that the hyperthermophilic crenarchaeote Sulfolobus spp. use a novel cell division system that consists of homologues of eukaryotic endosomal secretion complex required for transport III (ESCRT-III) proteins.

  • Comparative genomic analysis shows that Archaea possess at least three distinct membrane remodelling systems, namely, the FtsZ-based bacterial-type systems present in most Euryarchaeota, the ESCRT-III-based system that is responsible for cell division in the Desulphorococcales and the Sulfolobales, and a putative novel system centred around the archaeal actin-related protein in the Thermoproteales.

  • Many archaeal genomes, in particular those of 'Candidatus Korarchaeum cryptophilum', the Thaumarchaeota and some of the Thermococci, encode assortments of components from different membrane remodelling systems.

  • Evolutionary reconstructions suggest that the last common ancestor of the extant archaea possessed a complex membrane remodelling apparatus, different components of which were lost during subsequent evolution of archaeal lineages.

  • Eukaryotes seem to have inherited the ancestral membrane remodelling systems in their entire complexity.

Abstract

Recently a novel cell division system comprised of homologues of eukaryotic ESCRT-III (endosomal sorting complex required for transport III) proteins was discovered in the hyperthermophilic crenarchaeote Sulfolobus acidocaldarius. On the basis of this discovery, we undertook a comparative genomic analysis of the machineries for cell division and vesicle formation in Archaea. Archaea possess at least three distinct membrane remodelling systems: the FtsZ-based bacterial-type system, the ESCRT-III-based eukaryote-like system and a putative novel system that uses an archaeal actin-related protein. Many archaeal genomes encode assortments of components from different systems. Evolutionary reconstruction from these findings suggests that the last common ancestor of the extant Archaea possessed a complex membrane remodelling apparatus, different components of which were lost during subsequent evolution of archaeal lineages. By contrast, eukaryotes seem to have inherited all three ancestral systems.

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Figure 1: Representative gene neighbourhoods of known and predicted membrane remodelling and cell division systems in the Archaea.
Figure 2: The distribution of the key components of membrane manipulation systems among the Archaea.
Figure 3: A hypothetical evolutionary scenario for archaeal and eukaryotic membrane remodelling systems.

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Acknowledgements

The authors thank Y. Wolf for useful discussions and help with the preparation of figure 3. The authors' research is supported by the Intramural Research Program of the US National Institutes of Health, National Library of Medicine (K.S.M., N.Y. and E.V.K.) and by the Edward Penley Abraham Trust (S.D.B.).

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Authors and Affiliations

  1. National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, 20894, Maryland, USA

    Kira S. Makarova, Natalya Yutin & Eugene V. Koonin

  2. Sir William Dunn School of Pathology, South Parks Road, Oxford, OX1 3RE, UK

    Stephen D. Bell

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Correspondence to Stephen D. Bell or Eugene V. Koonin.

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Supplementary information

Supplementary information S1 (box)

The NCBI Refseq database1 was used for retrieval of information on genomic context. (PDF 100 kb)

Supplementary information S2 (table)

Central components of various cell division and membrane remodelling systems (XLS 57 kb)

Supplementary information S3 (figure)

MIT domains of VSP4 ATPase (PDF 138 kb)

Supplementary information S4 (figure)

Architecture of operons of all organisms mentioned in this Analysis article (PDF 250 kb)

Supplementary information S5 (table)

Neighbourhoods of all genes relevant to this work with genome context and gene coordinates (XLS 131 kb)

Supplementary information S6 (table)

Uncharacterized putative components of membrane remodelling systems in archaea (PDF 175 kb)

Supplementary information S7 (figure)

Alignment of Snf7 family proteins (PDF 93 kb)

Supplementary information S8 (figure)

Phylogenetic tree of VPS4 and related ATPases (PDF 209 kb)

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FURTHER INFORMATION

Stephen D. Bell's homepage

Eugene V. Koonin's homepage

arCOG

Glossary

Orthologue

One of two or more homologous genes (or the encoded proteins) that are derived by vertical descent from a common ancestor.

Paralogue

One of two or more homologous genes (or their encoded proteins) that have evolved following duplication of an ancestral gene.

FHA domain

A domain that binds phosphopeptides. Most FHA domains recognize phosphothreonine, with additional specificity contributed by residues that are carboxy–terminal to the phosphothreonine.

AAA+ ATPase

A member of the vast superfamily of ATPases associated with various cellular activities (AAA+). These proteins utilize the energy of ATP binding, hydrolysis and release to remodel macromolecular substrates.

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Makarova, K., Yutin, N., Bell, S. et al. Evolution of diverse cell division and vesicle formation systems in Archaea. Nat Rev Microbiol 8, 731–741 (2010). https://doi.org/10.1038/nrmicro2406

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