Single-cell genomics uncover Pelagibacter as the putative host of the extremely abundant uncultured 37-F6 viral population in the ocean

Abstract

The identification of relevant virus-host pairs that globally account for a large pool of carbon and nutrients in the ocean is paramount to build accurate ecological models. A previous work using single-virus genomics led to the discovery of the uncultured single-virus vSAG 37-F6, originally sorted from the Mediterranean Sea (Blanes Bay Microbial Observatory), that represents one of the most abundant dsDNA viral population in the marine surface virosphere. Here, from same sampling site, we report that a Pelagibacter single-cell contained a viral member of vSAG 37-F6 population, by means of PCR screening of sorted, genome-amplified single cells with vSAG 37-F6-specific primers and whole-genome sequencing. Furthermore, viruses from this population were also found in three other Pelagibacter single cells from the South Pacific and Atlantic oceans. These new uncultured pelagiphages were genetically different from the previously characterized pelagiphage isolates. Data showed that the uncultured vSAG 37-F6 population represents the Pelagibacter phages that inhabit the sunlit ocean better, and contains a vast unrecognized microdiversity.

Expanding the diversity of bacterioplankton isolates and modeling isolation efficacy with large scale dilution-to-extinction cultivation

“…One possibility is as an effective defense mechanism against abundant viruses. Viruses infecting SAR11 have been shown to be extremely abundant in both marine (115, 116) and freshwater (117) systems. Indeed, the paradox of high viral abundances and high host abundances in SAR11 has led to a refining of negative density dependent selection through Lokta-Volterra predator-prey dynamics (118) to include heterogeneous susceptibility at the strain level (119, 120) and positive density dependent selection through intraspecific proliferation of defense mechanisms (121).…”

Diel cycling of the cosmopolitan abundant Pelagibacter virus 37‐F6: one of the most abundant viruses on earth

“…However, none of these previously reported transcriptomic studies addressed the diel cycling of potentially the most abundant and cosmopolitan marine dsDNA virus in surface ocean, named virus vSAG 37-F6 (Martinez-Hernandez et al, 2017). This Pelagibacter virus was discovered by applying a novel single-virus genomic (SVG) approach (Martinez-Hernandez et al, 2017;Martinez-Hernandez et al, 2019a) around the same time of the publication of these reports (Aylward et al, 2017;Yoshida et al, 2018). The SVG-based technology enabled the discovery of some of the most abundant marine viral species in surface ocean (Martinez-Hernandez et al, 2017).…”

“…In addition, most of these viral contigs from Osaka Bay related to vSAG 37‐F6 had the specific capsid marker gene, representing viral group 37‐F6 (gene 9), which was the most abundant marine viral protein (Brum et al ., ; Martinez‐Hernandez et al ., ). The amino acid similarity of that shared capsid hallmark gene ranged from 72% to 95%, within values obtained previously for other reported 37‐F6 viral relatives found in single‐cells or cloned in fosmids (Martinez‐Hernandez et al ., , ). Among all assembled viral contigs from Osaka Bay, the virus OBV_N00758 was the closest one to vSAG 37‐F6 (Fig.…”

Long-read viral metagenomics enables capture of abundant and microdiverse viral populations and their niche-defining genomic islands

“…For example, the globally dominant members of the chemoheterotrophic order Pelagibacterales comprise up to 25% of all bacterioplankton and are major contributors to carbon remineralisation (Giovannoni, 2017). Their associated viruses dominate global oceans (Zhao et al, 2013;Martinez-Hernandez et al, 2018) and are likely to contribute significantly to carbon turnover in surface water by release of labile intracellular carbon during lysis (Suttle, 2005(Suttle, , 2007. However, the genomes of viruses associated with Pelagibacterales contain numerous GIs and/or high microdiversity (Zhao et al, 2013;Martinez-Hernandez et al, 2018).…”

“…Their associated viruses dominate global oceans (Zhao et al, 2013;Martinez-Hernandez et al, 2018) and are likely to contribute significantly to carbon turnover in surface water by release of labile intracellular carbon during lysis (Suttle, 2005(Suttle, , 2007. However, the genomes of viruses associated with Pelagibacterales contain numerous GIs and/or high microdiversity (Zhao et al, 2013;Martinez-Hernandez et al, 2018). Such features cause genome fragmentation in short-read assembly methods, resulting in reduced representation in the datasets following size-selection of contigs for downstream analyses (Martinez-Hernandez et al, 2017;Roux et al, 2017).…”