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Title: Ecogenomics of virophages and their giant virus hosts assessed through time series metagenomics

Abstract

Virophages are small viruses that co-infect eukaryotic cells alongside giant viruses (Mimiviridae) and hijack their machinery to replicate. While two types of virophages have been isolated, their genomic diversity and ecology remain largely unknown. Here we use time series metagenomics to identify and study the dynamics of 25 uncultivated virophage populations, 17 of which represented by complete or near-complete genomes, in two North American freshwater lakes. Taxonomic analysis suggests that these freshwater virophages represent at least three new candidate genera. Ecologically, virophage populations are repeatedly detected over years and evolutionary stable, yet their distinct abundance profiles and gene content suggest that virophage genera occupy different ecological niches. Co-occurrence analyses reveal 11 virophages strongly associated with uncultivated Mimiviridae, and three associated with eukaryotes among the Dinophyceae, Rhizaria, Alveolata, and Cryptophyceae groups. Together, these findings significantly augment virophage databases, help refine virophage taxonomy, and establish baseline ecological hypotheses and tools to study virophages in nature.

Authors:
 [1];  [2];  [2];  [2];  [3];  [4]
  1. The Ohio State Univ., Columbus, OH (United States). Dept. of Microbiology
  2. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  3. Univ. of Wisconsin, Madison, WI (United States). Dept. of Bacteriology. Dept. of Civil and Environmental Engineering
  4. The Ohio State Univ., Columbus, OH (United States). Dept. of Microbiology. Dept. of Civil, Environmental and Geodetic Engineering
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC); National Science Foundation (NSF); Gordon and Betty Moore Foundation (United States)
OSTI Identifier:
1459396
Grant/Contract Number:  
AC02-05CH11231; MCB-0702395; DEB-1344254; DEB-1440297; OCE-1536989; GBMF #3790
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 8; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; freshwater ecology; metagenomics; microbial ecology; phage biology

Citation Formats

Roux, Simon, Chan, Leong-Keat, Egan, Rob, Malmstrom, Rex R., McMahon, Katherine D., and Sullivan, Matthew B. Ecogenomics of virophages and their giant virus hosts assessed through time series metagenomics. United States: N. p., 2017. Web. doi:10.1038/s41467-017-01086-2.
Roux, Simon, Chan, Leong-Keat, Egan, Rob, Malmstrom, Rex R., McMahon, Katherine D., & Sullivan, Matthew B. Ecogenomics of virophages and their giant virus hosts assessed through time series metagenomics. United States. https://doi.org/10.1038/s41467-017-01086-2
Roux, Simon, Chan, Leong-Keat, Egan, Rob, Malmstrom, Rex R., McMahon, Katherine D., and Sullivan, Matthew B. Wed . "Ecogenomics of virophages and their giant virus hosts assessed through time series metagenomics". United States. https://doi.org/10.1038/s41467-017-01086-2. https://www.osti.gov/servlets/purl/1459396.
@article{osti_1459396,
title = {Ecogenomics of virophages and their giant virus hosts assessed through time series metagenomics},
author = {Roux, Simon and Chan, Leong-Keat and Egan, Rob and Malmstrom, Rex R. and McMahon, Katherine D. and Sullivan, Matthew B.},
abstractNote = {Virophages are small viruses that co-infect eukaryotic cells alongside giant viruses (Mimiviridae) and hijack their machinery to replicate. While two types of virophages have been isolated, their genomic diversity and ecology remain largely unknown. Here we use time series metagenomics to identify and study the dynamics of 25 uncultivated virophage populations, 17 of which represented by complete or near-complete genomes, in two North American freshwater lakes. Taxonomic analysis suggests that these freshwater virophages represent at least three new candidate genera. Ecologically, virophage populations are repeatedly detected over years and evolutionary stable, yet their distinct abundance profiles and gene content suggest that virophage genera occupy different ecological niches. Co-occurrence analyses reveal 11 virophages strongly associated with uncultivated Mimiviridae, and three associated with eukaryotes among the Dinophyceae, Rhizaria, Alveolata, and Cryptophyceae groups. Together, these findings significantly augment virophage databases, help refine virophage taxonomy, and establish baseline ecological hypotheses and tools to study virophages in nature.},
doi = {10.1038/s41467-017-01086-2},
journal = {Nature Communications},
number = ,
volume = 8,
place = {United States},
year = {2017},
month = {10}
}

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Figures / Tables:

Fig. 1 Fig. 1: Phylogeny and summarized gene content of virophage genomes. The maximum-likelihood phylogenetic tree was computed from a concatenated alignment of four core genes (major and minor capsid proteins, DNA packaging enzyme, and Cysteine protease). SH-like support are indicated on nodes, and branches with < 50% support are displayed asmore » multifurcations. The detection of key virophage genes is indicated for each genome on the right side. These key genes are classified as “core” (detected in all but one genome), ‘near-core’ (detected in > 68% of virophage genomes), and ‘signature genes’, i.e., genes specific to and detected in all members of known and newly proposed virophage genera. A question mark denotes the absence of genes similar to the DNA packaging enzyme in contig TBE_1002136, which is likely due to this genome being only a partial assembly, based on the comparison of this genome with the closely related TBE_1000887 (Supplementary Fig. 3). Six core genes previously identified from the comparison of isolate virophage« less

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Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.