Single-virus genomics reveals hidden cosmopolitan and abundant viruses

Francisco Martinez-Hernandez,Josefa Anton,Monica Lluesma Gomez,Oscar Fornas,Riccardo Rosselli,Maria Jose De La Cruz Peña,Manuel Martinez-Garcia,Matthew B Sullivan,Silvia G Acinas,Francisco Rodriguez-Valera,Benjamin Bolduc,Joaquín Martínez Martínez,Josep M Gasol

doi:10.1038/ncomms15892

Abstract

Microbes drive ecosystems under constraints imposed by viruses. However, a lack of virus genome information hinders our ability to answer fundamental, biological questions concerning microbial communities. Here we apply single-virus genomics (SVGs) to assess whether portions of marine viral communities are missed by current techniques. The majority of the here-identified 44 viral single-amplified genomes (vSAGs) are more abundant in global ocean virome data sets than published metagenome-assembled viral genomes or isolates. This indicates that vSAGs likely best represent the dsDNA viral populations dominating the oceans. Species-specific recruitment patterns and virome simulation data suggest that vSAGs are highly microdiverse and that microdiversity hinders the metagenomic assembly, which could explain why their genomes have not been identified before. Altogether, SVGs enable the discovery of some of the likely most abundant and ecologically relevant marine viral species, such as vSAG 37-F6, which were overlooked by other methodologies.

Highlights

Microbes drive ecosystems under constraints imposed by viruses
whole-genome amplification (WGA) of the sorted single viral particles yielded a total of 392 marine viral single-amplified genomes (Table 1; Supplementary Fig. 4 and Supplementary Note 1)
Compared to viral genome fragments assembled from the recent Global Oceanic Virome (GOV) metagenomics data set[2], our 37 viral single-amplified genomes (vSAGs) representing putative new viral species were at the ‘core’ of virus clusters (VCs) in the global marine viral network (Fig. 1; Supplementary Fig. 7 and Supplementary Tables 2–4)

Summary

Introduction

Microbes drive ecosystems under constraints imposed by viruses. a lack of virus genome information hinders our ability to answer fundamental, biological questions concerning microbial communities. Broader metagenomic surveys in the context of the Tara Oceans expeditions have unveiled ocean viral community patterns at a global scale[3] and provided a map of abundant, double-stranded DNA viruses with a total of 15,222 epipelagic and mesopelagic viral populations, comprising 867 major viral clusters, each corresponding to approximately genus-level groupings[2] Such studies emphasize the large disparity with cultivation efforts, as o1% of the observed viral populations are represented in culture[2,3,10,11]. Single-cell genomics (SCGs) has enabled sequencing of individual genomes of many abundant and ecologically important prokaryotes in marine and other environments[12,13,14,15,16] by disentangling the genetic complexity of the community to the minimum level, the cell This powerful approach has opened up new frontiers that overcome some of the metagenomic assembly limitations and culture biases. We employ single-virus genomics (SVGs) to natural marine viral assemblages from the Mediterranean Sea (epi- and mesopelagic) and the deep Atlantic Ocean, and demonstrate the power of this approach to uncover the genomics of some of the most abundant marine viruses

Methods

Results

Conclusion