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

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

doi:10.1038/ismej.2013.59

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 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.

Highlights

Viruses are thought to be extremely abundant in the sea
Our results suggest that marine Nucleo-cytoplasmic large DNA viruses (NCLDVs) probably outnumber eukaryotic organisms in the photic layer and that metagenomic sequence analyses promise to shed new light on the biodiversity of marine viruses and their interactions with potential hosts
Nucleo-cytoplasmic large DNA viruses (NCLDVs; Iyer et al, 2006, Yutin and Koonin, 2012) constitute an apparently monophyletic group of eukaryotic viruses with a large double-stranded DNA genome ranging from 100 kb up to 1.26 Mb

Summary

Introduction

Viruses are thought to be extremely abundant in the sea. phages alone outnumber all other life forms in seawater, reflecting the abundance of their. The the population dynamics of their unicellular algal abundance of EhVs could reach over 107 viruses mlÀ 1 host, which forms seasonal harmful blooms in coastal in rapidly expanding host populations in mesocosm areas (Tomaru et al, 2004) Another well-known virus experiments simulating host blooms (Schroeder (Emiliania huxleyi viruses (EhV)) controls the popula- et al, 2003, Pagarete et al, 2011). Since the discovery of the giant Mimivirus from tional multidisciplinary scientific program aiming fresh water samples, NCLDVs have become a subject to characterize ocean plankton diversity, the role of of broader interest This has led to several conceptual these drifting microorganisms in marine ecosystems breakthroughs in our understanding of the origin of and their response to environmental changes viruses and their links to the evolution of cellular (Karsenti et al, 2011). During the reach 104 viruses ml À 1 in natural sea water during expedition, planktonic organisms ranging in size from the period of host blooms (Tomaru et al, 2004). viruses to fish larvae together with physico-chemical

43 Indian Ocean

Results

Discussion