Deep sea sediments associated with cold seeps are a subsurface reservoir of viral diversity

Zexin Li,Chuwen Zhang,Yong Wang,Lu Zhang,Casey R J Hubert,Donald Pan,Xiyang Dong,Guangshan Wei,Yongyi Peng,Jiang-Hai Wang,Weiling Pi

doi:10.1038/s41396-021-00932-y

Abstract

In marine ecosystems, viruses exert control on the composition and metabolism of microbial communities, influencing overall biogeochemical cycling. Deep sea sediments associated with cold seeps are known to host taxonomically diverse microbial communities, but little is known about viruses infecting these microorganisms. Here, we probed metagenomes from seven geographically diverse cold seeps across global oceans to assess viral diversity, virus–host interaction, and virus-encoded auxiliary metabolic genes (AMGs). Gene-sharing network comparisons with viruses inhabiting other ecosystems reveal that cold seep sediments harbour considerable unexplored viral diversity. Most cold seep viruses display high degrees of endemism with seep fluid flux being one of the main drivers of viral community composition. In silico predictions linked 14.2% of the viruses to microbial host populations with many belonging to poorly understood candidate bacterial and archaeal phyla. Lysis was predicted to be a predominant viral lifestyle based on lineage-specific virus/host abundance ratios. Metabolic predictions of prokaryotic host genomes and viral AMGs suggest that viruses influence microbial hydrocarbon biodegradation at cold seeps, as well as other carbon, sulfur and nitrogen cycling via virus-induced mortality and/or metabolic augmentation. Overall, these findings reveal the global diversity and biogeography of cold seep viruses and indicate how viruses may manipulate seep microbial ecology and biogeochemistry.

Highlights

Marine cold seeps are typically found at the edges of continental shelves and feature mainly gaseous and liquid hydrocarbons from deep geologic sources [1, 2]
Though some cold seep viral OTUs (vOTUs) were very abundant in multiple sediment samples, a large majority (84%) of vOTUs were only present within a single cold seep site (Supplementary Table 5)
Further analysis of viral distribution across the seven cold seep sites (ANOSIM, R = 0.80, p = 0.001; Fig. 2a) shows that cold seep viruses display a high degree of endemism, similar to what was found previously in methane seep prokaryotic communities [74]

Summary

Introduction

Marine cold seeps are typically found at the edges of continental shelves and feature mainly gaseous and liquid hydrocarbons from deep geologic sources [1, 2]. Cold seeps are chemosynthetic ecosystems and contain an extensive diversity of archaea and bacteria which play important roles in hydrocarbon metabolism [6, 7] These microbial populations are highly active in influencing seep biogeochemistry at the sediment-water interface [8], and contribute to a variety of biological processes such as sulfate reduction, sulfur oxidation, denitrification, metal reduction and methanogenesis within the seabed [2, 8]. Novel viruses have been discovered in methane seep sediments, including a novel sister clade to the Microvirus genus of Enterobacteria phage and a putative archaeal virus linked to an anaerobic methane-oxidizing (ANME) clade [10, 11] These findings suggest that cold seeps harbour abundant and undiscovered viruses potentially influencing their microbial hosts and biogeochemical cycling at cold seeps

Methods

Results

Conclusion