Abstract

Oceanic viruses that infect bacteria, or phages, are known to modulate host diversity, metabolisms, and biogeochemical cycling, while the viruses that infect marine Archaea remain understudied despite the critical ecosystem roles played by their hosts. Here we introduce “MArVD”, for Metagenomic Archaeal Virus Detector, an annotation tool designed to identify putative archaeal virus contigs in metagenomic datasets. MArVD is made publicly available through the online iVirus analytical platform. Benchmarking analysis of MArVD showed it to be >99% accurate and 100% sensitive in identifying the 127 known archaeal viruses among the 12,499 viruses in the VirSorter curated dataset. Application of MArVD to 10 viral metagenomes from two depth profiles in the Eastern Tropical North Pacific (ETNP) oxygen minimum zone revealed 43 new putative archaeal virus genomes and large genome fragments ranging in size from 10 to 31 kb. Network-based classifications, which were consistent with marker gene phylogenies where available, suggested that these putative archaeal virus contigs represented six novel candidate genera. Ecological analyses, via fragment recruitment and ordination, revealed that the diversity and relative abundances of these putative archaeal viruses were correlated with oxygen concentration and temperature along two OMZ-spanning depth profiles, presumably due to structuring of the host Archaea community. Peak viral diversity and abundances were found in surface waters, where Thermoplasmata 16S rRNA genes are prevalent, suggesting these archaea as hosts in the surface habitats. Together these findings provide a baseline for identifying archaeal viruses in sequence datasets, and an initial picture of the ecology of such viruses in non-extreme environments.

Highlights

  • IntroductionPhages, are relatively well-studied in the oceans and are thought to infect approximately one-third of seawater microbes at any given time (reviewed in Brum & Sullivan, 2015)

  • Viruses that infect bacteria, or phages, are relatively well-studied in the oceans and are thought to infect approximately one-third of seawater microbes at any given time

  • To identify archaeal virus contigs in viromes, we developed the Metagenomic archaeal virus detector (MArVD) that identifies putative archaeal virus contigs based on a ‘‘majority rules’’ consensus taxonomic assignment drawn from the taxonomic annotation of each predicted gene (Fig. S1)

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Summary

Introduction

Phages, are relatively well-studied in the oceans and are thought to infect approximately one-third of seawater microbes at any given time (reviewed in Brum & Sullivan, 2015). Phages alter microbial community structure and ecosystem functioning through host cell lysis. Some phages hijack their host’s metabolic machinery (Vos et al, 2009), reviewed in Hurwitz & U’Ren (2016), which alters host cell metabolite concentrations (Ankrah et al, 2014; Dendooven et al, 2016), and can have direct impacts on ecosystem critical microbial metabolisms including carbon fixation, redox potential, nitrogen and sulfur cycling, and archaeal ammonia oxidation (Hurwitz, Hallam & Sullivan, 2013; Puxty et al, 2016; Thompson et al, 2011; Lindell et al, 2005; Roux et al, 2016; Anantharaman et al, 2014). The evolutionary trajectories of phages and their hosts are intimately connected via an arms race for infection or resistance mechanisms (Comeau & Krisch, 2005; Stern & Sorek, 2011; Stoddard, Martiny & Marston, 2007; Koskella & Brockhurst, 2014)

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