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Diversity and distribution of viruses inhabiting the deepest ocean on Earth

Abstract

As the most abundant biological entities on the planet, viruses significantly influence the overall functioning of marine ecosystems. The abundance, distribution, and biodiversity of viral communities in the upper ocean have been relatively well studied, but our understanding of viruses in the hadal biosphere remains poor. Here, we established the oceanic trench viral genome dataset (OTVGD) by analysing 19 microbial metagenomes derived from seawater and sediment samples of the Mariana, Yap, and Kermadec Trenches. The trench viral communities harbored remarkably high novelty, and they were predicted to infect ecologically important microbial clades, including Thaumarchaeota and Oleibacter. Significant inter-trench and intra-trench exchange of viral communities was proposed. Moreover, viral communities in different habitats (seawater/sediment and depth-stratified ocean zones) exhibited distinct niche-dependent distribution patterns and genomic properties. Notably, microbes and viruses in the hadopelagic seawater seemed to preferably adopt lysogenic lifestyles compared to those in the upper ocean. Furthermore, niche-specific auxiliary metabolic genes were identified in the hadal viral genomes, and a novel viral D-amino acid oxidase was functionally and phylogenetically characterized, suggesting the contribution of these genes in the utilization of refractory organic matter. Together, these findings highlight the genomic novelty, dynamic movement, and environment-driven diversification of viral communities in oceanic trenches, and suggest that viruses may influence the hadal ecosystem by reprogramming the metabolism of their hosts and modulating the community of keystone microbes.

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Fig. 1: Overview of the oceanic trench viral genome dataset (OTVGD).
Fig. 2: Connectivity of viruses in the oceanic trenches.
Fig. 3: Abundance profiles and genomic features of oceanic trench viruses.
Fig. 4: Lysogenic lifestyle of the viruses in seawater of the Mariana Trench.
Fig. 5: Characterization of auxiliary metabolic genes (AMGs) in hadal viruses.

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Acknowledgements

This work was financially supported by the National Key R&D Program of China (2018YFC0309800), and the National Natural Science Foundation of China (grants 91851113, 41921006, 41776173, and 41676118).

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H.J. and X.X. conceived and designed the study. Y.Y., J.W., and H.J. conducted the bioinformatic analyses and data visualization. Y.H., S.W., and C.M. performed functional analysis of AMG. Y.H., and M.Z. helped in collecting hadal microbial genome data. Y.Z. participated in statistical analysis. H.J. and Y.Y. interpreted the data and drafted the manuscript. Y.W. and H.J. provided useful suggestions to improve the manuscript. X.X. supervised the project. All the authors reviewed the results and approved the manuscript.

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Correspondence to Xiang Xiao.

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Jian, H., Yi, Y., Wang, J. et al. Diversity and distribution of viruses inhabiting the deepest ocean on Earth. ISME J (2021). https://doi.org/10.1038/s41396-021-00994-y

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