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Title: Diversity, evolution, and classification of virophages uncovered through global metagenomics

Abstract

BACKGROUND: Virophages are small viruses with double-stranded DNA genomes that replicate along with giant viruses and co-infect eukaryotic cells. Due to the paucity of virophage reference genomes, a collective understanding of the global virophage diversity, distribution, and evolution is lacking. RESULTS: Here we screened a public collection of over 14,000 metagenomes using the virophage-specific major capsid protein (MCP) as "bait." We identified 44,221 assembled virophage sequences, of which 328 represent high-quality (complete or near-complete) genomes from diverse habitats including the human gut, plant rhizosphere, and terrestrial subsurface. Comparative genomic analysis confirmed the presence of four core genes in a conserved block. We used these genes to establish a revised virophage classification including 27 clades with consistent genome length, gene content, and habitat distribution. Moreover, for eight high-quality virophage genomes, we computationally predicted putative eukaryotic virus hosts. CONCLUSION: Overall, our approach has increased the number of known virophage genomes by 10-fold and revealed patterns of genome evolution and global virophage distribution. We anticipate that the expanded diversity presented here will provide the backbone for further virophage studies.

Authors:
ORCiD logo [1];  [1];  [1];  [1];  [2];  [1];  [3];  [4];  [1];  [1];  [1];  [1];  [1]
  1. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  2. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); BSRC Alexander Fleming", Athens (Greece)
  3. Univ. of Wisconsin, Madison, WI (United States)
  4. Concordia Univ., Montreal, QC (Canada)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1591848
Grant/Contract Number:  
[AC02-05CH11231]
Resource Type:
Accepted Manuscript
Journal Name:
Microbiome
Additional Journal Information:
[ Journal Volume: 7; Journal Issue: 1]; Journal ID: ISSN 2049-2618
Publisher:
BioMed Central
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; metagenomics; virophage; major capsid protein (MCP); virophage classification; virophage-NCLDV interactions; global distribution

Citation Formats

Paez-Espino, David, Zhou, Jinglie, Roux, Simon, Nayfach, Stephen, Pavlopoulos, Georgios A., Schulz, Frederik, McMahon, Katherine D., Walsh, David, Woyke, Tanja, Ivanova, Natalia N., Eloe-Fadrosh, Emiley A., Tringe, Susannah G., and Kyrpides, Nikos C. Diversity, evolution, and classification of virophages uncovered through global metagenomics. United States: N. p., 2019. Web. doi:10.1186/s40168-019-0768-5.
Paez-Espino, David, Zhou, Jinglie, Roux, Simon, Nayfach, Stephen, Pavlopoulos, Georgios A., Schulz, Frederik, McMahon, Katherine D., Walsh, David, Woyke, Tanja, Ivanova, Natalia N., Eloe-Fadrosh, Emiley A., Tringe, Susannah G., & Kyrpides, Nikos C. Diversity, evolution, and classification of virophages uncovered through global metagenomics. United States. doi:10.1186/s40168-019-0768-5.
Paez-Espino, David, Zhou, Jinglie, Roux, Simon, Nayfach, Stephen, Pavlopoulos, Georgios A., Schulz, Frederik, McMahon, Katherine D., Walsh, David, Woyke, Tanja, Ivanova, Natalia N., Eloe-Fadrosh, Emiley A., Tringe, Susannah G., and Kyrpides, Nikos C. Tue . "Diversity, evolution, and classification of virophages uncovered through global metagenomics". United States. doi:10.1186/s40168-019-0768-5. https://www.osti.gov/servlets/purl/1591848.
@article{osti_1591848,
title = {Diversity, evolution, and classification of virophages uncovered through global metagenomics},
author = {Paez-Espino, David and Zhou, Jinglie and Roux, Simon and Nayfach, Stephen and Pavlopoulos, Georgios A. and Schulz, Frederik and McMahon, Katherine D. and Walsh, David and Woyke, Tanja and Ivanova, Natalia N. and Eloe-Fadrosh, Emiley A. and Tringe, Susannah G. and Kyrpides, Nikos C.},
abstractNote = {BACKGROUND: Virophages are small viruses with double-stranded DNA genomes that replicate along with giant viruses and co-infect eukaryotic cells. Due to the paucity of virophage reference genomes, a collective understanding of the global virophage diversity, distribution, and evolution is lacking. RESULTS: Here we screened a public collection of over 14,000 metagenomes using the virophage-specific major capsid protein (MCP) as "bait." We identified 44,221 assembled virophage sequences, of which 328 represent high-quality (complete or near-complete) genomes from diverse habitats including the human gut, plant rhizosphere, and terrestrial subsurface. Comparative genomic analysis confirmed the presence of four core genes in a conserved block. We used these genes to establish a revised virophage classification including 27 clades with consistent genome length, gene content, and habitat distribution. Moreover, for eight high-quality virophage genomes, we computationally predicted putative eukaryotic virus hosts. CONCLUSION: Overall, our approach has increased the number of known virophage genomes by 10-fold and revealed patterns of genome evolution and global virophage distribution. We anticipate that the expanded diversity presented here will provide the backbone for further virophage studies.},
doi = {10.1186/s40168-019-0768-5},
journal = {Microbiome},
number = [1],
volume = [7],
place = {United States},
year = {2019},
month = {12}
}

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