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A novel group of diverse Polinton-like viruses discovered by metagenome analysis.
BMC Biol. 2015 Nov 11; 13:95.BB

Abstract

BACKGROUND

The rapidly growing metagenomic databases provide increasing opportunities for computational discovery of new groups of organisms. Identification of new viruses is particularly straightforward given the comparatively small size of viral genomes, although fast evolution of viruses complicates the analysis of novel sequences. Here we report the metagenomic discovery of a distinct group of diverse viruses that are distantly related to the eukaryotic virus-like transposons of the Polinton superfamily.

RESULTS

The sequence of the putative major capsid protein (MCP) of the unusual linear virophage associated with Phaeocystis globosa virus (PgVV) was used as a bait to identify potential related viruses in metagenomic databases. Assembly of the contigs encoding the PgVV MCP homologs followed by comprehensive sequence analysis of the proteins encoded in these contigs resulted in the identification of a large group of Polinton-like viruses (PLV) that resemble Polintons (polintoviruses) and virophages in genome size, and share with them a conserved minimal morphogenetic module that consists of major and minor capsid proteins and the packaging ATPase. With a single exception, the PLV lack the retrovirus-type integrase that is encoded in the genomes of all Polintons and the Mavirus group of virophages. However, some PLV encode a newly identified tyrosine recombinase-integrase that is common in bacteria and bacteriophages and is also found in the Organic Lake virophage group. Although several PLV genomes and individual genes are integrated into algal genomes, it appears likely that most of the PLV are viruses. Given the absence of protease and retrovirus-type integrase, the PLV could resemble the ancestral polintoviruses that evolved from bacterial tectiviruses. Apart from the conserved minimal morphogenetic module, the PLV widely differ in their genome complements but share a gene network with Polintons and virophages, suggestive of multiple gene exchanges within a shared gene pool.

CONCLUSIONS

The discovery of PLV substantially expands the emerging class of eukaryotic viruses and transposons that also includes Polintons and virophages. This class of selfish elements is extremely widespread and might have been a hotbed of eukaryotic virus, transposon and plasmid evolution. New families of these elements are expected to be discovered.

Authors+Show Affiliations

National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD, 20894, USA.National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD, 20894, USA.National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD, 20894, USA.Unité Biologie Moléculaire du Gène chez les Extrêmophiles, Department of Microbiology, Institut Pasteur, Paris, France.National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD, 20894, USA. koonin@ncbi.nlm.nih.gov.

Pub Type(s)

Journal Article
Research Support, N.I.H., Intramural

Language

eng

PubMed ID

26560305

Citation

Yutin, Natalya, et al. "A Novel Group of Diverse Polinton-like Viruses Discovered By Metagenome Analysis." BMC Biology, vol. 13, 2015, p. 95.
Yutin N, Shevchenko S, Kapitonov V, et al. A novel group of diverse Polinton-like viruses discovered by metagenome analysis. BMC Biol. 2015;13:95.
Yutin, N., Shevchenko, S., Kapitonov, V., Krupovic, M., & Koonin, E. V. (2015). A novel group of diverse Polinton-like viruses discovered by metagenome analysis. BMC Biology, 13, 95. https://doi.org/10.1186/s12915-015-0207-4
Yutin N, et al. A Novel Group of Diverse Polinton-like Viruses Discovered By Metagenome Analysis. BMC Biol. 2015 Nov 11;13:95. PubMed PMID: 26560305.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - A novel group of diverse Polinton-like viruses discovered by metagenome analysis. AU - Yutin,Natalya, AU - Shevchenko,Sofiya, AU - Kapitonov,Vladimir, AU - Krupovic,Mart, AU - Koonin,Eugene V, Y1 - 2015/11/11/ PY - 2015/08/14/received PY - 2015/10/28/accepted PY - 2015/11/13/entrez PY - 2015/11/13/pubmed PY - 2016/7/7/medline SP - 95 EP - 95 JF - BMC biology JO - BMC Biol VL - 13 N2 - BACKGROUND: The rapidly growing metagenomic databases provide increasing opportunities for computational discovery of new groups of organisms. Identification of new viruses is particularly straightforward given the comparatively small size of viral genomes, although fast evolution of viruses complicates the analysis of novel sequences. Here we report the metagenomic discovery of a distinct group of diverse viruses that are distantly related to the eukaryotic virus-like transposons of the Polinton superfamily. RESULTS: The sequence of the putative major capsid protein (MCP) of the unusual linear virophage associated with Phaeocystis globosa virus (PgVV) was used as a bait to identify potential related viruses in metagenomic databases. Assembly of the contigs encoding the PgVV MCP homologs followed by comprehensive sequence analysis of the proteins encoded in these contigs resulted in the identification of a large group of Polinton-like viruses (PLV) that resemble Polintons (polintoviruses) and virophages in genome size, and share with them a conserved minimal morphogenetic module that consists of major and minor capsid proteins and the packaging ATPase. With a single exception, the PLV lack the retrovirus-type integrase that is encoded in the genomes of all Polintons and the Mavirus group of virophages. However, some PLV encode a newly identified tyrosine recombinase-integrase that is common in bacteria and bacteriophages and is also found in the Organic Lake virophage group. Although several PLV genomes and individual genes are integrated into algal genomes, it appears likely that most of the PLV are viruses. Given the absence of protease and retrovirus-type integrase, the PLV could resemble the ancestral polintoviruses that evolved from bacterial tectiviruses. Apart from the conserved minimal morphogenetic module, the PLV widely differ in their genome complements but share a gene network with Polintons and virophages, suggestive of multiple gene exchanges within a shared gene pool. CONCLUSIONS: The discovery of PLV substantially expands the emerging class of eukaryotic viruses and transposons that also includes Polintons and virophages. This class of selfish elements is extremely widespread and might have been a hotbed of eukaryotic virus, transposon and plasmid evolution. New families of these elements are expected to be discovered. SN - 1741-7007 UR - https://www.unboundmedicine.com/medline/citation/26560305/A_novel_group_of_diverse_Polinton_like_viruses_discovered_by_metagenome_analysis_ L2 - https://bmcbiol.biomedcentral.com/articles/10.1186/s12915-015-0207-4 DB - PRIME DP - Unbound Medicine ER -