Viral community analysis in a marine oxygen minimum zone indicates increased potential for viral manipulation of microbial physiological state

Sophie K Jurgensen,Matthew B Sullivan,Jennifer R Brum,Simon Roux,Frank J Stewart,Sarah M Schwenck

doi:10.1038/s41396-021-01143-1

Abstract

Microbial communities in oxygen minimum zones (OMZs) are known to have significant impacts on global biogeochemical cycles, but viral influence on microbial processes in these regions are much less studied. Here we provide baseline ecological patterns using microscopy and viral metagenomics from the Eastern Tropical North Pacific (ETNP) OMZ region that enhance our understanding of viruses in these climate-critical systems. While extracellular viral abundance decreased below the oxycline, viral diversity and lytic infection frequency remained high within the OMZ, demonstrating that viral influences on microbial communities were still substantial without the detectable presence of oxygen. Viral community composition was strongly related to oxygen concentration, with viral populations in low-oxygen portions of the water column being distinct from their surface layer counterparts. However, this divergence was not accompanied by the expected differences in viral-encoded auxiliary metabolic genes (AMGs) relating to nitrogen and sulfur metabolisms that are known to be performed by microbial communities in these low-oxygen and anoxic regions. Instead, several abundant AMGs were identified in the oxycline and OMZ that may modulate host responses to low-oxygen stress. We hypothesize that this is due to selection for viral-encoded genes that influence host survivability rather than modulating host metabolic reactions within the ETNP OMZ. Together, this study shows that viruses are not only diverse throughout the water column in the ETNP, including the OMZ, but their infection of microorganisms has the potential to alter host physiological state within these biogeochemically important regions of the ocean.

Highlights

Marine viruses are recognized to play key roles in marine ecosystems by lysing ~10–40% of bacteria per day, recycling organic matter and nutrients via the ‘viral shunt’, and contributing to microbial niche differentiation through horizontal gene transfer [1,2,3,4]
The results from this study indicate that while viral diversity and infection frequency remain high within the Eastern Tropical North Pacific (ETNP) oxygen minimum zones (OMZs), the structure of the viral community and the composition of viralencoded auxiliary metabolic genes (AMGs) are substantially altered in the oxycline and the functionally anoxic core of the OMZ
The most abundant virulence gene, a glycosyl- were shared among the depth categories, their relative abundances transferase involved in the biosynthesis of lipopolysaccharide, indicate strong selection for different viral-encoded AMGs with contains an endotoxin in some Gram-negative bacteria including varying oxygen concentration that are not related to nitrogen or Pseudomonas [97,98,99]

Summary

Introduction

Marine viruses are recognized to play key roles in marine ecosystems by lysing ~10–40% of bacteria per day, recycling organic matter and nutrients via the ‘viral shunt’, and contributing to microbial niche differentiation through horizontal gene transfer [1,2,3,4]. The increased FIC in the OMZ indicated that viruses mixed layer communities and the low-oxygen communities, were still lytically replicating in the OMZ as has been observed in respectively, and their subtle differences in relative abundance multiple prior studies [28, 29, 33,34,35], resulting in a lack of of viral populations was visualized using a heatmap (Supplemencorrelation with oxygen concentration (Supplementary Fig. S3).

Results

Conclusion