Environmental Viral Genomes Shed New Light on Virus-Host Interactions in the Ocean

ABSTRACT Metagenomics has revealed the existence of numerous uncharacterized viral lineages, which are referred to as viral “dark matter.” However, our knowledge regarding viral genomes is biased toward culturable viruses. In this study, we analyzed 1,600 (1,352 nonredundant) complete double-strande...

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Autores principales:	Yosuke Nishimura, Hiroyasu Watai, Takashi Honda, Tomoko Mihara, Kimiho Omae, Simon Roux, Romain Blanc-Mathieu, Keigo Yamamoto, Pascal Hingamp, Yoshihiko Sako, Matthew B. Sullivan, Susumu Goto, Hiroyuki Ogata, Takashi Yoshida
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	genome marine ecosystem metabolism metagenomics virus Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/88ce285c047343e0ad1bb6b4aca94c22
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spelling	oai:doaj.org-article:88ce285c047343e0ad1bb6b4aca94c222021-11-15T15:21:46ZEnvironmental Viral Genomes Shed New Light on Virus-Host Interactions in the Ocean10.1128/mSphere.00359-162379-5042https://doaj.org/article/88ce285c047343e0ad1bb6b4aca94c222017-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00359-16https://doaj.org/toc/2379-5042ABSTRACT Metagenomics has revealed the existence of numerous uncharacterized viral lineages, which are referred to as viral “dark matter.” However, our knowledge regarding viral genomes is biased toward culturable viruses. In this study, we analyzed 1,600 (1,352 nonredundant) complete double-stranded DNA viral genomes (10 to 211 kb) assembled from 52 marine viromes. Together with 244 previously reported uncultured viral genomes, a genome-wide comparison delineated 617 genus-level operational taxonomic units (OTUs) for these environmental viral genomes (EVGs). Of these, 600 OTUs contained no representatives from known viruses, thus putatively corresponding to novel viral genera. Predicted hosts of the EVGs included major groups of marine prokaryotes, such as marine group II Euryarchaeota and SAR86, from which no viruses have been isolated to date, as well as Flavobacteriaceae and SAR116. Our analysis indicates that marine cyanophages are already well represented in genome databases and that one of the EVGs likely represents a new cyanophage lineage. Several EVGs encode many enzymes that appear to function for an efficient utilization of iron-sulfur clusters or to enhance host survival. This suggests that there is a selection pressure on these marine viruses to accumulate genes for specific viral propagation strategies. Finally, we revealed that EVGs contribute to a 4-fold increase in the recruitment of photic-zone viromes compared with the use of current reference viral genomes. IMPORTANCE Viruses are diverse and play significant ecological roles in marine ecosystems. However, our knowledge of genome-level diversity in viruses is biased toward those isolated from few culturable hosts. Here, we determined 1,352 nonredundant complete viral genomes from marine environments. Lifting the uncertainty that clouds short incomplete sequences, whole-genome-wide analysis suggests that these environmental genomes represent hundreds of putative novel viral genera. Predicted hosts include dominant groups of marine bacteria and archaea with no isolated viruses to date. Some of the viral genomes encode many functionally related enzymes, suggesting a strong selection pressure on these marine viruses to control cellular metabolisms by accumulating genes.Yosuke NishimuraHiroyasu WataiTakashi HondaTomoko MiharaKimiho OmaeSimon RouxRomain Blanc-MathieuKeigo YamamotoPascal HingampYoshihiko SakoMatthew B. SullivanSusumu GotoHiroyuki OgataTakashi YoshidaAmerican Society for Microbiologyarticlegenomemarine ecosystemmetabolismmetagenomicsvirusMicrobiologyQR1-502ENmSphere, Vol 2, Iss 2 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	genome marine ecosystem metabolism metagenomics virus Microbiology QR1-502
spellingShingle	genome marine ecosystem metabolism metagenomics virus Microbiology QR1-502 Yosuke Nishimura Hiroyasu Watai Takashi Honda Tomoko Mihara Kimiho Omae Simon Roux Romain Blanc-Mathieu Keigo Yamamoto Pascal Hingamp Yoshihiko Sako Matthew B. Sullivan Susumu Goto Hiroyuki Ogata Takashi Yoshida Environmental Viral Genomes Shed New Light on Virus-Host Interactions in the Ocean
description	ABSTRACT Metagenomics has revealed the existence of numerous uncharacterized viral lineages, which are referred to as viral “dark matter.” However, our knowledge regarding viral genomes is biased toward culturable viruses. In this study, we analyzed 1,600 (1,352 nonredundant) complete double-stranded DNA viral genomes (10 to 211 kb) assembled from 52 marine viromes. Together with 244 previously reported uncultured viral genomes, a genome-wide comparison delineated 617 genus-level operational taxonomic units (OTUs) for these environmental viral genomes (EVGs). Of these, 600 OTUs contained no representatives from known viruses, thus putatively corresponding to novel viral genera. Predicted hosts of the EVGs included major groups of marine prokaryotes, such as marine group II Euryarchaeota and SAR86, from which no viruses have been isolated to date, as well as Flavobacteriaceae and SAR116. Our analysis indicates that marine cyanophages are already well represented in genome databases and that one of the EVGs likely represents a new cyanophage lineage. Several EVGs encode many enzymes that appear to function for an efficient utilization of iron-sulfur clusters or to enhance host survival. This suggests that there is a selection pressure on these marine viruses to accumulate genes for specific viral propagation strategies. Finally, we revealed that EVGs contribute to a 4-fold increase in the recruitment of photic-zone viromes compared with the use of current reference viral genomes. IMPORTANCE Viruses are diverse and play significant ecological roles in marine ecosystems. However, our knowledge of genome-level diversity in viruses is biased toward those isolated from few culturable hosts. Here, we determined 1,352 nonredundant complete viral genomes from marine environments. Lifting the uncertainty that clouds short incomplete sequences, whole-genome-wide analysis suggests that these environmental genomes represent hundreds of putative novel viral genera. Predicted hosts include dominant groups of marine bacteria and archaea with no isolated viruses to date. Some of the viral genomes encode many functionally related enzymes, suggesting a strong selection pressure on these marine viruses to control cellular metabolisms by accumulating genes.
format	article
author	Yosuke Nishimura Hiroyasu Watai Takashi Honda Tomoko Mihara Kimiho Omae Simon Roux Romain Blanc-Mathieu Keigo Yamamoto Pascal Hingamp Yoshihiko Sako Matthew B. Sullivan Susumu Goto Hiroyuki Ogata Takashi Yoshida
author_facet	Yosuke Nishimura Hiroyasu Watai Takashi Honda Tomoko Mihara Kimiho Omae Simon Roux Romain Blanc-Mathieu Keigo Yamamoto Pascal Hingamp Yoshihiko Sako Matthew B. Sullivan Susumu Goto Hiroyuki Ogata Takashi Yoshida
author_sort	Yosuke Nishimura
title	Environmental Viral Genomes Shed New Light on Virus-Host Interactions in the Ocean
title_short	Environmental Viral Genomes Shed New Light on Virus-Host Interactions in the Ocean
title_full	Environmental Viral Genomes Shed New Light on Virus-Host Interactions in the Ocean
title_fullStr	Environmental Viral Genomes Shed New Light on Virus-Host Interactions in the Ocean
title_full_unstemmed	Environmental Viral Genomes Shed New Light on Virus-Host Interactions in the Ocean
title_sort	environmental viral genomes shed new light on virus-host interactions in the ocean
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/88ce285c047343e0ad1bb6b4aca94c22
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Environmental Viral Genomes Shed New Light on Virus-Host Interactions in the Ocean

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