A multi-omics approach to microbial nitrogen and sulfur cycling in the oxygen starved ocean

Microbial communities mediate biogeochemical processes of Carbon (C), Nitrogen (N) and Sulfur (S) cycling in the ocean on global scales. Oxygen (O₂) availability is a key driver in these processes and shapes microbial community structure and metabolisms. As O₂ decreases, microbes utilize alternative terminal electron acceptors, nitrate (NO₃–), nitrite, sulfate and carbon dioxide, depleting biologically available nitrogen and producing greenhouse gases nitrous oxide (N₂O) and methane (CH₄). Marine oxygen minimum zones (OMZs) are areas of O₂-depletion (O₂ < 20µM) in sub-surface waters due to the respiration of organic matter from the surface. In areas of acute O₂-depletion or where OMZs contact underlying sediments, hydrogen sulfide (H₂S) and CH₄ accumulate within OMZ waters, drastically altering microbial community structure and metabolism. In this thesis, I explore microbial cycles along defined gradients of O₂, NO₃- and H₂S in Saanich Inlet, a seasonally anoxic fjord on the coast of British Columbia Canada. I develop a time-resolved multi-omic dataset consisting of small subunit ribosomal RNA amplicon sequences, single cell amplified genomes (SAGs), metagenomes, -transcriptomes and -proteomes, coupled with geochemical measurements, enabling robust microbial metabolic reconstruction at the individual, population and community levels of organization. Using metaproteomics, I construct a conceptual model of metabolic interactions involving N and S cycling, and carbon fixation, forming the basis for a collaborative effort to build a gene-centric numerical model, identifying an unrecognized niche for N₂O reduction. Using single cell amplified genomes (SAGs) from Saanich Inlet, I identify genes for N₂O reduction, nosZ, within the dark matter phylum Marinimicrobia clade SHBH1141, filling the proposed niche of non-denitrifying N₂O-reducers. Using globally sourced Marinimicrobia SAGs, I further analyze energy metabolism and biogeography of several Marinimicrobia clades, revealing roles in C, N and S cycling along eco-thermodynamic gradients throughout the ocean. Finally, I chart the global abundance and distribution of nosZ genes and transcripts within the ocean, identifying previously unappreciated potential sinks for N₂O. As OMZs continue to expand and intensify due to climate change, defining metabolic processes and interactions along gradients of O₂-depletion becomes increasingly important. This thesis provides foundational knowledge related to the microbial communities driving coupled biogeochemical cycling in OMZs. [This dissertation was updated to include a missing chapter on 2018-10-05.]

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