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.]