Exploring nucleo-cytoplasmic large DNA viruses in Tara Oceans microbial metagenomes

Nucleo-cytoplasmic large DNA viruses (NCLDVs) constitute a group of eukaryotic viruses that can have crucial ecological roles in the sea by accelerating the turnover of their unicellular hosts or by causing diseases in animals. To better characterize the diversity, abundance and biogeography of mari...

Full description

Bibliographic Details
Main Authors: Hingamp, Pascal, Grimsley, Nigel, Acinas, Silvia G, Clerissi, Camille, Subirana, Lucie, Poulain, Julie, Ferrera, Isabel, Sarmento, Hugo, Villar, Emilie, Lima-Mendez, Gipsi, Faust, Karoline, Sunagawa, Shinichi, Claverie, Jean-Michel, Moreau, Hervé, Desdevises, Yves, Bork, Peer, Raes, Jeroen, de Vargas, Colomban, Karsenti, Eric, Kandels-Lewis, Stefanie, Jaillon, Olivier, Not, Fabrice, Pesant, Stéphane, Wincker, Patrick, Ogata, Hiroyuki
Format: Online
Language:English
Published: Nature Publishing Group 2013
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3749498/
id pubmed-3749498
recordtype oai_dc
spelling pubmed-37494982013-09-01 Exploring nucleo-cytoplasmic large DNA viruses in Tara Oceans microbial metagenomes Hingamp, Pascal Grimsley, Nigel Acinas, Silvia G Clerissi, Camille Subirana, Lucie Poulain, Julie Ferrera, Isabel Sarmento, Hugo Villar, Emilie Lima-Mendez, Gipsi Faust, Karoline Sunagawa, Shinichi Claverie, Jean-Michel Moreau, Hervé Desdevises, Yves Bork, Peer Raes, Jeroen de Vargas, Colomban Karsenti, Eric Kandels-Lewis, Stefanie Jaillon, Olivier Not, Fabrice Pesant, Stéphane Wincker, Patrick Ogata, Hiroyuki Original Article Nucleo-cytoplasmic large DNA viruses (NCLDVs) constitute a group of eukaryotic viruses that can have crucial ecological roles in the sea by accelerating the turnover of their unicellular hosts or by causing diseases in animals. To better characterize the diversity, abundance and biogeography of marine NCLDVs, we analyzed 17 metagenomes derived from microbial samples (0.2–1.6 μm size range) collected during the Tara Oceans Expedition. The sample set includes ecosystems under-represented in previous studies, such as the Arabian Sea oxygen minimum zone (OMZ) and Indian Ocean lagoons. By combining computationally derived relative abundance and direct prokaryote cell counts, the abundance of NCLDVs was found to be in the order of 104–105 genomes ml−1 for the samples from the photic zone and 102–103 genomes ml−1 for the OMZ. The Megaviridae and Phycodnaviridae dominated the NCLDV populations in the metagenomes, although most of the reads classified in these families showed large divergence from known viral genomes. Our taxon co-occurrence analysis revealed a potential association between viruses of the Megaviridae family and eukaryotes related to oomycetes. In support of this predicted association, we identified six cases of lateral gene transfer between Megaviridae and oomycetes. Our results suggest that marine NCLDVs probably outnumber eukaryotic organisms in the photic layer (per given water mass) and that metagenomic sequence analyses promise to shed new light on the biodiversity of marine viruses and their interactions with potential hosts. Nature Publishing Group 2013-09 2013-04-11 /pmc/articles/PMC3749498/ /pubmed/23575371 http://dx.doi.org/10.1038/ismej.2013.59 Text en Copyright © 2013 International Society for Microbial Ecology http://creativecommons.org/licenses/by/3.0/ This work is licensed under a Creative Commons Attribution 3.0 Unported License. To view a copy of this license, visit http://creativecommons.org/licenses/by/3.0/
repository_type Open Access Journal
institution_category Foreign Institution
institution US National Center for Biotechnology Information
building NCBI PubMed
collection Online Access
language English
format Online
author Hingamp, Pascal
Grimsley, Nigel
Acinas, Silvia G
Clerissi, Camille
Subirana, Lucie
Poulain, Julie
Ferrera, Isabel
Sarmento, Hugo
Villar, Emilie
Lima-Mendez, Gipsi
Faust, Karoline
Sunagawa, Shinichi
Claverie, Jean-Michel
Moreau, Hervé
Desdevises, Yves
Bork, Peer
Raes, Jeroen
de Vargas, Colomban
Karsenti, Eric
Kandels-Lewis, Stefanie
Jaillon, Olivier
Not, Fabrice
Pesant, Stéphane
Wincker, Patrick
Ogata, Hiroyuki
spellingShingle Hingamp, Pascal
Grimsley, Nigel
Acinas, Silvia G
Clerissi, Camille
Subirana, Lucie
Poulain, Julie
Ferrera, Isabel
Sarmento, Hugo
Villar, Emilie
Lima-Mendez, Gipsi
Faust, Karoline
Sunagawa, Shinichi
Claverie, Jean-Michel
Moreau, Hervé
Desdevises, Yves
Bork, Peer
Raes, Jeroen
de Vargas, Colomban
Karsenti, Eric
Kandels-Lewis, Stefanie
Jaillon, Olivier
Not, Fabrice
Pesant, Stéphane
Wincker, Patrick
Ogata, Hiroyuki
Exploring nucleo-cytoplasmic large DNA viruses in Tara Oceans microbial metagenomes
author_facet Hingamp, Pascal
Grimsley, Nigel
Acinas, Silvia G
Clerissi, Camille
Subirana, Lucie
Poulain, Julie
Ferrera, Isabel
Sarmento, Hugo
Villar, Emilie
Lima-Mendez, Gipsi
Faust, Karoline
Sunagawa, Shinichi
Claverie, Jean-Michel
Moreau, Hervé
Desdevises, Yves
Bork, Peer
Raes, Jeroen
de Vargas, Colomban
Karsenti, Eric
Kandels-Lewis, Stefanie
Jaillon, Olivier
Not, Fabrice
Pesant, Stéphane
Wincker, Patrick
Ogata, Hiroyuki
author_sort Hingamp, Pascal
title Exploring nucleo-cytoplasmic large DNA viruses in Tara Oceans microbial metagenomes
title_short Exploring nucleo-cytoplasmic large DNA viruses in Tara Oceans microbial metagenomes
title_full Exploring nucleo-cytoplasmic large DNA viruses in Tara Oceans microbial metagenomes
title_fullStr Exploring nucleo-cytoplasmic large DNA viruses in Tara Oceans microbial metagenomes
title_full_unstemmed Exploring nucleo-cytoplasmic large DNA viruses in Tara Oceans microbial metagenomes
title_sort exploring nucleo-cytoplasmic large dna viruses in tara oceans microbial metagenomes
description Nucleo-cytoplasmic large DNA viruses (NCLDVs) constitute a group of eukaryotic viruses that can have crucial ecological roles in the sea by accelerating the turnover of their unicellular hosts or by causing diseases in animals. To better characterize the diversity, abundance and biogeography of marine NCLDVs, we analyzed 17 metagenomes derived from microbial samples (0.2–1.6 μm size range) collected during the Tara Oceans Expedition. The sample set includes ecosystems under-represented in previous studies, such as the Arabian Sea oxygen minimum zone (OMZ) and Indian Ocean lagoons. By combining computationally derived relative abundance and direct prokaryote cell counts, the abundance of NCLDVs was found to be in the order of 104–105 genomes ml−1 for the samples from the photic zone and 102–103 genomes ml−1 for the OMZ. The Megaviridae and Phycodnaviridae dominated the NCLDV populations in the metagenomes, although most of the reads classified in these families showed large divergence from known viral genomes. Our taxon co-occurrence analysis revealed a potential association between viruses of the Megaviridae family and eukaryotes related to oomycetes. In support of this predicted association, we identified six cases of lateral gene transfer between Megaviridae and oomycetes. Our results suggest that marine NCLDVs probably outnumber eukaryotic organisms in the photic layer (per given water mass) and that metagenomic sequence analyses promise to shed new light on the biodiversity of marine viruses and their interactions with potential hosts.
publisher Nature Publishing Group
publishDate 2013
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3749498/
_version_ 1612004809431318528