Giant Viruses Encode Actin-Related Proteins

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Abstract

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.

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Most cited references 39

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The New Tree of Eukaryotes

Fabien Burki, Andrew Roger, Matthew W Brown … (2019)

For 15 years, the eukaryote Tree of Life (eToL) has been divided into five to eight major groupings, known as 'supergroups'. However, the tree has been profoundly rearranged during this time. The new eToL results from the widespread application of phylogenomics and numerous discoveries of major lineages of eukaryotes, mostly free-living heterotrophic protists. The evidence that supports the tree has transitioned from a synthesis of molecular phylogenetics and biological characters to purely molecular phylogenetics. Most current supergroups lack defining morphological or cell-biological characteristics, making the supergroup label even more arbitrary than before. Going forward, the combination of traditional culturing with maturing culture-free approaches and phylogenomics should accelerate the process of completing and resolving the eToL at its deepest levels.

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Asgard archaea illuminate the origin of eukaryotic cellular complexity

Katarzyna Zaremba-Niedzwiedzka, Eva F. Caceres, Jimmy Saw … (2017)

The origin and cellular complexity of eukaryotes represent a major enigma in biology. Current data support scenarios in which an archaeal host cell and an alphaproteobacterial (mitochondrial) endosymbiont merged together, resulting in the first eukaryotic cell. The host cell is related to Lokiarchaeota, an archaeal

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Global Organization and Proposed Megataxonomy of the Virus World

Eugene V. Koonin, Valerian Dolja, Mart Krupovic … (2020)

Viruses and mobile genetic elements are molecular parasites or symbionts that coevolve with nearly all forms of cellular life. The route of virus replication and protein expression is determined by the viral genome type. Comparison of these routes led to the classification of viruses into seven “Baltimore classes” (BCs) that define the major features of virus reproduction. However, recent phylogenomic studies identified multiple evolutionary connections among viruses within each of the BCs as well as between different classes. Due to the modular organization of virus genomes, these relationships defy simple representation as lines of descent but rather form complex networks. Phylogenetic analyses of virus hallmark genes combined with analyses of gene-sharing networks show that replication modules of five BCs (three classes of RNA viruses and two classes of reverse-transcribing viruses) evolved from a common ancestor that encoded an RNA-directed RNA polymerase or a reverse transcriptase. Bona fide viruses evolved from this ancestor on multiple, independent occasions via the recruitment of distinct cellular proteins as capsid subunits and other structural components of virions. The single-stranded DNA (ssDNA) viruses are a polyphyletic class, with different groups evolving by recombination between rolling-circle-replicating plasmids, which contributed the replication protein, and positive-sense RNA viruses, which contributed the capsid protein. The double-stranded DNA (dsDNA) viruses are distributed among several large monophyletic groups and arose via the combination of distinct structural modules with equally diverse replication modules. Phylogenomic analyses reveal the finer structure of evolutionary connections among RNA viruses and reverse-transcribing viruses, ssDNA viruses, and large subsets of dsDNA viruses. Taken together, these analyses allow us to outline the global organization of the virus world. Here, we describe the key aspects of this organization and propose a comprehensive hierarchical taxonomy of viruses.

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Contributors

Emma Teeling: Role: Associate Editor

Journal

Journal ID (nlm-ta): Mol Biol Evol

Journal ID (iso-abbrev): Mol Biol Evol

Journal ID (publisher-id): molbev

Title: Molecular Biology and Evolution

Publisher: Oxford University Press

ISSN (Print): 0737-4038

ISSN (Electronic): 1537-1719

Publication date Collection: February 2022

Publication date (Electronic): 12 February 2022

Publication date PMC-release: 12 February 2022

Volume: 39

Issue: 2

Electronic Location Identifier: msac022

Affiliations

[1 ] CEA, CNRS, Institute for Integrative Biology of the Cell (I2BC), Université Paris-Saclay , Gif-sur-Yvette, France

[2 ] Génomique Métabolique, Génoscope, Institut François Jacob, CEA, CNRS, Université d’Évry, Université Paris-Saclay , Evry, France

[3 ] Institute for Chemical Research, Kyoto University , Gokasho, Uji, Japan

[4 ] Research Federation for the Study of Global Ocean Systems Ecology and Evolution , Tara Oceans, France

[5 ] Département de Microbiologie, Institut Pasteur , Paris, France

Author notes

[†]

Violette Da Cunha and Morgan Gaia contributed equally to this work.

Corresponding authors: E-mails: violette.da.cunha.vdc@ 123456gmail.com ; patrick.forterre@ 123456pasteur.fr .

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Hiroyuki Ogata https://orcid.org/0000-0001-6594-377X

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Publisher ID: msac022

DOI: 10.1093/molbev/msac022

PMC ID: 8850707

PubMed ID: 35150280

SO-VID: d6d01b60-23f2-44ac-861c-b5278e6645e4

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This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License ( https://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com

Giant Viruses Encode Actin-Related Proteins

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Most cited references 39

The New Tree of Eukaryotes

Asgard archaea illuminate the origin of eukaryotic cellular complexity

Global Organization and Proposed Megataxonomy of the Virus World

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