Microorganisms oxidize organic nitrogen to nitrate in a series of steps. Nitrite, an intermediate product, accumulates at the base of the sunlit layer in the subtropical ocean, forming a primary nitrite maximum, but can accumulate throughout the sunlit layer at higher latitudes. We model nitrifying chemoautotrophs in a marine ecosystem and demonstrate that microbial community interactions can explain the nitrite distributions. Our theoretical framework proposes that nitrite can accumulate to a higher concentration than ammonium because of differences in underlying redox chemistry and cell size between ammonia- and nitrite-oxidizing chemoautotrophs. Using ocean circulation models, we demonstrate that nitrifying microorganisms are excluded in the sunlit layer when phytoplankton are nitrogen-limited, but thrive at depth when phytoplankton become light-limited, resulting in nitrite accumulation there. However, nitrifying microorganisms may coexist in the sunlit layer when phytoplankton are iron- or light-limited (often in higher latitudes). These results improve understanding of the controls on nitrification, and provide a framework for representing chemoautotrophs and their biogeochemical effects in ocean models.

Significance: Organic matter in the global ocean, soils, and sediments stores about five times more carbon than the atmosphere. Thus, the controls on the accumulation of organic matter are critical to global carbon cycling. However, we lack a quantitative understanding of these controls. This prevents meaningful descriptions of organic matter cycling in global climate models, which are required for understanding how changes in organic matter reservoirs provide feedbacks to past and present changes in climate. Currently, explanations for organic matter accumulation remain under debate, characterized by seemingly competing hypotheses. Here, we develop a quantitative framework for organic matter accumulation that unifies these hypotheses. The framework derives from the ecological dynamics of microorganisms, the dominant consumers of organic matter.

Significance: Prochlorococcus is the smallest and most abundant photosynthetic organism on Earth and is thought to be confined to low-latitude regions by its requirement for warm waters. Latitudinal transects in the North Pacific, however, demonstrate that the poleward decrease of this species occurs across a wide range of temperatures. An additional mechanism is likely required. We use theory, computational models, and additional observational data to suggest that the poleward decrease is caused by an ecological interaction: a shared predator which consumes both Prochlorococcus and similar-sized heterotrophic bacteria. Understanding the fate of this organism requires a knowledge of the interconnected ecosystem of other organisms, where both direct and indirect interactions control community structure.

Microbial activity mediates the fluxes of greenhouse gases. However, in the global models of the marine and terrestrial biospheres used for climate change projections, typically only photosynthetic microbial activity is resolved mechanistically. To move forward, we argue that global biogeochemical models need a theoretically grounded framework with which to constrain parameterizations of diverse microbial metabolisms. Here, we explain how the key redox chemistry underlying metabolisms provides a path towards this goal. Using this first-principles approach, the presence or absence of metabolic functional types emerges dynamically from ecological interactions, expanding model applicability to unobserved environments.“Nothing is less real than realism. It is only by selection, by elimination, by emphasis, that we get at the real meaning of things.” –Georgia O’Keefe

Mechanistic description of the transition from aerobic to anaerobic metabolism is necessary for diagnostic and predictive modeling of fixed nitrogen loss in anoxic marine zones (AMZs). In a metabolic model where diverse oxygen- and nitrogen-cycling microbial metabolisms are described by underlying redox chemical reactions, we predict a transition from strictly aerobic to predominantly anaerobic regimes as the outcome of ecological interactions along an oxygen gradient, obviating the need for prescribed critical oxygen concentrations. Competing aerobic and anaerobic metabolisms can coexist in anoxic conditions whether these metabolisms represent obligate or facultative populations. In the coexistence regime, relative rates of aerobic and anaerobic activity are determined by the ratio of oxygen to electron donor supply. The model simulates key characteristics of AMZs, such as the accumulation of nitrite and the sustainability of anammox at higher oxygen concentrations than denitrification, and articulates how microbial biomass concentrations relate to associated water column transformation rates as a function of redox stoichiometry and energetics. Incorporating the metabolic model into an idealized two-dimensional ocean circulation results in a simulated AMZ, in which a secondary chlorophyll maximum emerges from oxygen-limited grazing, and where vertical mixing and dispersal in the oxycline also contribute to metabolic co-occurrence. The modeling approach is mechanistic yet computationally economical and suitable for global change applications.

Microorganisms in marine oxygen minimum zones (OMZs) drive globally impactful biogeochemical processes. One such process is multistep denitrification (NO ₃ ^– →NO ₂ ^– →NO→N ₂ O→N ₂ ), which dominates OMZ bioavailable nitrogen (N) loss and nitrous oxide (N ₂ O) 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 NO ₂ ^– and N ₂ O in a NO ₃ ^– -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 NO ₃ ^– →NO ₂ ^– 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 NO ₃ ^– →NO ₂ ^– module. Results also capture observations that NO ₃ ^– is the dominant source of N ₂ O. 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.