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

Pascal Hingamp; Nigel Grimsley; Silvia G. Acinas; Camille Clerissi; Lucie Subirana; Julie Poulain; Isabel Ferrera; Hugo Sarmento; Emilie Villar; Gipsi Lima-Mendez; Karoline Faust; Shinichi Sunagawa; Jean Michel Claverie; Hervé Moreau; Yves Desdevises; Peer Bork; Jeroen Raes; Colomban De Vargas; Eric Karsenti; Stefanie Kandels-Lewis; Olivier Jaillon; Fabrice Not; Stéphane Pesant; Patrick Wincker; Hiroyuki Ogata

doi:10.1038/ismej.2013.59

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

Pascal Hingamp, Nigel Grimsley, Silvia G. Acinas, Camille Clerissi, Lucie Subirana, Julie Poulain, Isabel Ferrera, Hugo Sarmento, Emilie Villar, Gipsi Lima-Mendez, Karoline Faust, Shinichi Sunagawa, Jean Michel Claverie, Hervé Moreau, Yves Desdevises, Peer Bork, Jeroen Raes, Colomban De Vargas, Eric Karsenti, Stefanie Kandels-LewisOlivier Jaillon, Fabrice Not, Stéphane Pesant, Patrick Wincker, Hiroyuki Ogata

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Abstract

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 10 4 -10 5 genomes ml -1 for the samples from the photic zone and 10 2 -10 3 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.

Original language	English
Pages (from-to)	1678-1695
Number of pages	18
Journal	ISME Journal
Volume	7
Issue number	9
DOIs	https://doi.org/10.1038/ismej.2013.59
Publication status	Published - Sept 2013
Externally published	Yes

Funding

We thank the coordinators and members of the Tara Oceans consortium (http://www.embl.de/tara-oceans/start/) for organizing sampling and data analysis. We thank the commitment of the following people and sponsors who made this singular expedition possible: CNRS, EMBL, Genoscope/CEA, VIB, Stazione Zoologica Anton Dohrn, UNIMIB, ANR (projects POSEIDON/ANR-09-BLAN-0348, BIOMARKS/ANR-08-BDVA-003, PROMETHEUS/ANR-09-GENM-031, and TARA-GIRUS/ANR-09-PCS-GENM-218), EU FP7 (MicroB3/No.287589), FWO, BIO5, Biosphere 2, agnès b., the Veolia Environment Foundation, Region Bretagne, World Courier, Illumina, Cap L’Orient, the EDF Foundation EDF Diversiterre, FRB, the Prince Albert II de Monaco Foundation, Etienne Bourgois, the Tara schooner and its captain and crew. CC benefited from a doctoral fellowship from the AXA Research Fund. Tara Oceans would not exist without the continuous support of the participating 23 institutes (see http://oceans.taraexpedi-tions.org). This article is contribution number 0003 of the Tara Oceans Expedition 2009–2012.

Keywords

eukaryotic viruses
marine NCLDVs
oomycetes
taxon co-occurrence

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1038/ismej.2013.59

ismej201359Final published version, 0.98 MBLicence: CC BY

Cite this

Hingamp, P., Grimsley, N., Acinas, S. G., Clerissi, C., Subirana, L., Poulain, J., Ferrera, I., Sarmento, H., Villar, E., Lima-Mendez, G., Faust, K., Sunagawa, S., Claverie, J. M., Moreau, H., Desdevises, Y., Bork, P., Raes, J., De Vargas, C., Karsenti, E., ... Ogata, H. (2013). Exploring nucleo-cytoplasmic large DNA viruses in Tara Oceans microbial metagenomes. ISME Journal, 7(9), 1678-1695. https://doi.org/10.1038/ismej.2013.59

@article{fc359957c3f643518f20663794475a90,

title = "Exploring nucleo-cytoplasmic large DNA viruses in Tara Oceans microbial metagenomes",

abstract = "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 10 4 -10 5 genomes ml -1 for the samples from the photic zone and 10 2 -10 3 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.",

keywords = "eukaryotic viruses, marine NCLDVs, oomycetes, taxon co-occurrence",

author = "Pascal Hingamp and Nigel Grimsley and Acinas, {Silvia G.} and Camille Clerissi and Lucie Subirana and Julie Poulain and Isabel Ferrera and Hugo Sarmento and Emilie Villar and Gipsi Lima-Mendez and Karoline Faust and Shinichi Sunagawa and Claverie, {Jean Michel} and Herv{\'e} Moreau and Yves Desdevises and Peer Bork and Jeroen Raes and {De Vargas}, Colomban and Eric Karsenti and Stefanie Kandels-Lewis and Olivier Jaillon and Fabrice Not and St{\'e}phane Pesant and Patrick Wincker and Hiroyuki Ogata",

note = "Funding Information: We thank the coordinators and members of the Tara Oceans consortium (http://www.embl.de/tara-oceans/start/) for organizing sampling and data analysis. We thank the commitment of the following people and sponsors who made this singular expedition possible: CNRS, EMBL, Genoscope/CEA, VIB, Stazione Zoologica Anton Dohrn, UNIMIB, ANR (projects POSEIDON/ANR-09-BLAN-0348, BIOMARKS/ANR-08-BDVA-003, PROMETHEUS/ANR-09-GENM-031, and TARA-GIRUS/ANR-09-PCS-GENM-218), EU FP7 (MicroB3/No.287589), FWO, BIO5, Biosphere 2, agn{\`e}s b., the Veolia Environment Foundation, Region Bretagne, World Courier, Illumina, Cap L{\textquoteright}Orient, the EDF Foundation EDF Diversiterre, FRB, the Prince Albert II de Monaco Foundation, Etienne Bourgois, the Tara schooner and its captain and crew. CC benefited from a doctoral fellowship from the AXA Research Fund. Tara Oceans would not exist without the continuous support of the participating 23 institutes (see http://oceans.taraexpedi-tions.org). This article is contribution number 0003 of the Tara Oceans Expedition 2009–2012.",

year = "2013",

month = sep,

doi = "10.1038/ismej.2013.59",

language = "English",

volume = "7",

pages = "1678--1695",

journal = "ISME Journal",

issn = "1751-7362",

publisher = "Oxford University Press",

number = "9",

}

Hingamp, P, Grimsley, N, Acinas, SG, Clerissi, C, Subirana, L, Poulain, J, Ferrera, I, Sarmento, H, Villar, E, Lima-Mendez, G, Faust, K, Sunagawa, S, Claverie, JM, Moreau, H, Desdevises, Y, Bork, P, Raes, J, De Vargas, C, Karsenti, E, Kandels-Lewis, S, Jaillon, O, Not, F, Pesant, S, Wincker, P & Ogata, H 2013, 'Exploring nucleo-cytoplasmic large DNA viruses in Tara Oceans microbial metagenomes', ISME Journal, vol. 7, no. 9, pp. 1678-1695. https://doi.org/10.1038/ismej.2013.59

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T1 - Exploring nucleo-cytoplasmic large DNA viruses in Tara Oceans microbial metagenomes

AU - Hingamp, Pascal

AU - Grimsley, Nigel

AU - Acinas, Silvia G.

AU - Clerissi, Camille

AU - Subirana, Lucie

AU - Poulain, Julie

AU - Ferrera, Isabel

AU - Sarmento, Hugo

AU - Villar, Emilie

AU - Lima-Mendez, Gipsi

AU - Faust, Karoline

AU - Sunagawa, Shinichi

AU - Claverie, Jean Michel

AU - Moreau, Hervé

AU - Desdevises, Yves

AU - Bork, Peer

AU - Raes, Jeroen

AU - De Vargas, Colomban

AU - Karsenti, Eric

AU - Kandels-Lewis, Stefanie

AU - Jaillon, Olivier

AU - Not, Fabrice

AU - Pesant, Stéphane

AU - Wincker, Patrick

AU - Ogata, Hiroyuki

N1 - Funding Information: We thank the coordinators and members of the Tara Oceans consortium (http://www.embl.de/tara-oceans/start/) for organizing sampling and data analysis. We thank the commitment of the following people and sponsors who made this singular expedition possible: CNRS, EMBL, Genoscope/CEA, VIB, Stazione Zoologica Anton Dohrn, UNIMIB, ANR (projects POSEIDON/ANR-09-BLAN-0348, BIOMARKS/ANR-08-BDVA-003, PROMETHEUS/ANR-09-GENM-031, and TARA-GIRUS/ANR-09-PCS-GENM-218), EU FP7 (MicroB3/No.287589), FWO, BIO5, Biosphere 2, agnès b., the Veolia Environment Foundation, Region Bretagne, World Courier, Illumina, Cap L’Orient, the EDF Foundation EDF Diversiterre, FRB, the Prince Albert II de Monaco Foundation, Etienne Bourgois, the Tara schooner and its captain and crew. CC benefited from a doctoral fellowship from the AXA Research Fund. Tara Oceans would not exist without the continuous support of the participating 23 institutes (see http://oceans.taraexpedi-tions.org). This article is contribution number 0003 of the Tara Oceans Expedition 2009–2012.

PY - 2013/9

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N2 - 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 10 4 -10 5 genomes ml -1 for the samples from the photic zone and 10 2 -10 3 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.

AB - 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 10 4 -10 5 genomes ml -1 for the samples from the photic zone and 10 2 -10 3 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.

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KW - marine NCLDVs

KW - oomycetes

KW - taxon co-occurrence

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SN - 1751-7362

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JO - ISME Journal

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ER -

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

Abstract

Funding

Keywords

UN SDGs

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