Ecological dynamics explain modular denitrification in the ocean

Microorganisms in marine oxygen minimum zones (OMZs) drive globally impactful biogeochemical processes. One such process is multistep denitrification (NO₃⁻→NO₂⁻→NO→N₂O→N₂), which dominates OMZ bioavailable nitrogen (N) loss and nitrous oxide (N₂O) production. Denitrification-derived N loss is typically measured and modeled as a single step, but observations reveal that most denitrifiers in OMZs contain subsets ("modules") of the complete pathway. Here, we identify the ecological mechanisms sustaining diverse denitrifiers, explain the prevalence of certain modules, and examine the implications for N loss. We describe microbial functional types carrying out diverse denitrification modules by their underlying redox chemistry, constraining their traits with thermodynamics and pathway length penalties, in an idealized OMZ ecosystem model. Biomass yields of single-step modules increase along the denitrification pathway when organic matter (OM) limits growth, which explains the viability of populations respiring NO₂⁻ and N₂O in a NO₃⁻-filled ocean. Results predict denitrifier community succession along environmental gradients: Pathway length increases as the limiting substrate shifts from OM to N, suggesting a niche for the short NO₃⁻→NO₂⁻ module in free-living, OM-limited communities, and for the complete pathway in organic particle-associated communities, consistent with observations. The model captures and mechanistically explains the observed dominance and higher oxygen tolerance of the NO₃⁻→NO₂⁻ module. Results also capture observations that NO₃⁻ is the dominant source of N₂O. Our framework advances the mechanistic understanding of the relationship between microbial ecology and N loss in the ocean and can be extended to other processes and environments.