Abstract
Viral diversity and virus-host interactions in oxygen-starved regions of the ocean, also known as oxygen minimum zones (OMZs), remain relatively unexplored. Microbial community metabolism in OMZs alters nutrient and energy flow through marine food webs, resulting in biological nitrogen loss and greenhouse gas production. Thus, viruses infecting OMZ microbes have the potential to modulate community metabolism with resulting feedback on ecosystem function. Here, we describe viral communities inhabiting oxic surface (10 m) and oxygen-starved basin (200 m) waters of Saanich Inlet, a seasonally anoxic fjord on the coast of Vancouver Island, British Columbia using viral metagenomics and complete viral fosmid sequencing on samples collected between April 2007 and April 2010. Of 6459 open reading frames (ORFs) predicted across all 34 viral fosmids, 77.6% (n = 5010) had no homology to reference viral genomes. These fosmids recruited a higher proportion of viral metagenomic sequences from Saanich Inlet than from nearby northeastern subarctic Pacific Ocean (Line P) waters, indicating differences in the viral communities between coastal and open ocean locations. While functional annotations of fosmid ORFs were limited, recruitment to NCBI's non-redundant “nr” database and publicly available single-cell genomes identified putative viruses infecting marine thaumarchaeal and SUP05 proteobacteria to provide potential host linkages with relevance to coupled biogeochemical cycling processes in OMZ waters. Taken together, these results highlight the power of coupled analyses of multiple sequence data types, such as viral metagenomic and fosmid sequence data with prokaryotic single cell genomes, to chart viral diversity, elucidate genomic and ecological contexts for previously unclassifiable viral sequences, and identify novel host interactions in natural and engineered ecosystems.
Highlights
The long evolutionary history of viruses with cellular life is evident from the diseases they cause, such as influenza and AIDS, and from the viral genes found in the genomes of cells
The genetic diversity of viral communities in the oxic and anoxic waters of Saanich Inlet was assessed through viral metagenomic data (Table S1) and large-insert fosmids (Table S3)
The fosmid sequences lacked similarity to known viral genomes as 5010 of 6459 (77.5%) open reading frames (ORFs) across all 34 viral fosmids had no significant homology to viral reference genomes
Summary
The long evolutionary history of viruses with cellular life is evident from the diseases they cause, such as influenza and AIDS, and from the viral genes found in the genomes of cells These relationships have their origins in viruses that infect bacteria, archaea and protists, all of which play a critical role in global nutrient and energy cycling and in maintaining functional ecosystems. Mining cellular metagenomic and single-cell genome datasets has unearthed new virus genomes and identified potential virus-host relationships (Anantharaman et al, 2014; Roux et al, 2014b) from previously uncultured hosts These inferred virus-host interactions reveal a past virus encounter and subsequent infection of a host organism and indicate the potential for genetic exchange during the infection cycle that can drive consequent effects on the metabolic status and rates of the infected host. When viral genomic data can be linked to a specific host organism, it becomes possible to study virus-host interactions within natural or engineered ecosystems and place “viral dark matter” into an ecological context
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