Abstract

Microbial communities are critical to ecosystem dynamics and biogeochemical cycling in the open oceans. Viruses are essential elements of these communities, influencing the productivity, diversity, and evolution of cellular hosts. To further explore the natural history and ecology of open-ocean viruses, we surveyed the spatiotemporal dynamics of double-stranded DNA (dsDNA) viruses in both virioplankton and bacterioplankton size fractions in the North Pacific Subtropical Gyre, one of the largest biomes on the planet. Assembly and clustering of viral genomes revealed a peak in virioplankton diversity at the base of the euphotic zone, where virus populations and host species richness both reached their maxima. Simultaneous characterization of both extracellular and intracellular viruses suggested depth-specific reproductive strategies. In particular, analyses indicated elevated lytic interactions in the mixed layer, more temporally variable temperate phage interactions at the base of the euphotic zone, and increased lysogeny in the mesopelagic ocean. Furthermore, the depth variability of auxiliary metabolic genes suggested habitat-specific strategies for viral influence on light-energy, nitrogen, and phosphorus acquisition during host infection. Most virus populations were temporally persistent over several years in this environment at the 95% nucleic acid identity level. In total, our analyses revealed variable distributional patterns and diverse reproductive and metabolic strategies of virus populations in the open-ocean water column.

Highlights

  • Viruses represent dynamic reservoirs of unexplored genetic diversity

  • Station ALOHA (22°45′ N, 158° W), a relatively seasonally stable environment located in the North Pacific Subtropical Gyre (NPSG), is a wellcharacterized sampling site of the Hawaii Ocean Timeseries (HOT) program

  • Our study recovered a large fraction of double-stranded DNA (dsDNA) viruses found at Station ALOHA, revealing a hotspot for microbial diversity at the base of the euphotic zone, where the majority of viruses were distinct from those previously reported

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Summary

Introduction

On average an order of magnitude more abundant than cellular organisms [1], viruses occur at ~107/mL in the surface layer of open oceans covering ~40% of Earth [2] In this environment, dsDNA bacteriophages infect key microbial groups, including oxygenic photoautotrophs such as Prochlorococcus and Synechococcus (e.g., [3, 4]) and common bacterial heterotrophs such as Pelagibacter (SAR11), Puniceispirillum (SAR116), Roseobacter, and Alteromonas (e.g., [5,6,7,8]). DsDNA bacteriophages infect key microbial groups, including oxygenic photoautotrophs such as Prochlorococcus and Synechococcus (e.g., [3, 4]) and common bacterial heterotrophs such as Pelagibacter (SAR11), Puniceispirillum (SAR116), Roseobacter, and Alteromonas (e.g., [5,6,7,8]) Viruses influence the diversity and biogeochemistry of marine ecosystems by carrying auxiliary metabolic genes (AMGs) that manipulate host metabolism during infection (reviewed in [13])

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