Discovery of several novel, widespread, and ecologically distinct marine Thaumarchaeota viruses that encode amoC nitrification genes

Abstract

Much of the diversity of prokaryotic viruses has yet to be described. In particular, there are no viral isolates that infect abundant, globally significant marine archaea including the phylum Thaumarchaeota. This phylum oxidizes ammonia, fixes inorganic carbon, and thus contributes to globally significant nitrogen and carbon cycles in the oceans. Metagenomics provides an alternative to culture-dependent means for identifying and characterizing viral diversity. Some viruses carry auxiliary metabolic genes (AMGs) that are acquired via horizontal gene transfer from their host(s), allowing inference of what host a virus infects. Here we present the discovery of 15 new genomically and ecologically distinct Thaumarchaeota virus populations, identified as contigs that encode viral capsid and thaumarchaeal ammonia monooxygenase genes (amoC). These viruses exhibit depth and latitude partitioning and are distributed globally in various marine habitats including pelagic waters, estuarine habitats, and hydrothermal plume water and sediments. We found evidence of viral amoC expression and that viral amoC AMGs sometimes comprise up to half of total amoC DNA copies in cellular fraction metagenomes, highlighting the potential impact of these viruses on N cycling in the oceans. Phylogenetics suggest they are potentially tailed viruses and share a common ancestor with related marine Euryarchaeota viruses. This work significantly expands our view of viruses of globally important marine Thaumarchaeota.

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Acknowledgements

We thank Cameron Thrash, Barbara Campbell, and Feng Chen for permission to include in our analysis select contigs from viral metagenomes sequenced at the Joint Genome Institute for which they are principal investigators. This work was supported by funding from The Gordon and Betty Moore Foundation Marine Microbiology Initiative (GBMF3779) to JAF; from the National Institutes of Health to NAA and JAF (R01 GM120624-01A1); and from the National Science Foundation OCE-1138368 to GR.

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Correspondence to Nathan A. Ahlgren.

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Ahlgren, N.A., Fuchsman, C.A., Rocap, G. et al. Discovery of several novel, widespread, and ecologically distinct marine Thaumarchaeota viruses that encode amoC nitrification genes. ISME J 13, 618–631 (2019) doi:10.1038/s41396-018-0289-4

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