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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.

© 2021. The Authors. Anaerobic microbial activity in the ocean causes losses of bioavailable nitrogen and emission of nitrous oxide to the atmosphere, but its predictability at global scales remains limited. Resource ratio theory suggests that anaerobic activity becomes sustainable when the ratio of oxygen to organic matter supply is below the ratio required by aerobic metabolisms. Here, we demonstrate the relevance of this framework at the global scale using three-dimensional ocean datasets, providing a new interpretation of existing observations. Evaluations of the location and extent of anoxic zones and a diagnostic rate of pelagic nitrogen loss are consistent with previous estimates. However, we demonstrate that a threshold based on substrate-supply fluxes is qualitatively different from a threshold based solely on the ambient oxygen concentration. This implies that use of the flux-based threshold in global biogeochemical models can result in different predictions of anaerobic activity and nitrogen loss.

Significance Robust predictions of future changes in global biogeochemical cycling require an understanding of how microorganisms adapt to stressful and changing environments. In the ocean, rates of adaptation will be a function of both evolutionary timescales and physical dynamics. However, little is known about this interaction. We examined evolutionary dynamics of marine microbes by combining a model of microbial adaptation with varying selection pressures with a high-resolution ocean circulation model. A trade-off emerged between two evolutionary strategies: (i) ability to adapt plastically to short-term environmental fluctuations with delayed genetic adaptation and (ii) more rapid genetic adaptation with limited response to short-term environmental fluctuations. This trade-off determines evolutionary timescales and provides a foundation for understanding distributions of microbial traits and biogeochemistry., Marine microbes form the base of ocean food webs and drive ocean biogeochemical cycling. Yet little is known about the ability of microbial populations to adapt as they are advected through changing conditions. Here, we investigated the interplay between physical and biological timescales using a model of adaptation and an eddy-resolving ocean circulation climate model. Two criteria were identified that relate the timing and nature of adaptation to the ratio of physical to biological timescales. Genetic adaptation was impeded in highly variable regimes by nongenetic modifications but was promoted in more stable environments. An evolutionary trade-off emerged where greater short-term nongenetic transgenerational effects (low-γ strategy) enabled rapid responses to environmental fluctuations but delayed genetic adaptation, while fewer short-term transgenerational effects (high-γ strategy) allowed faster genetic adaptation but inhibited short-term responses. Our results demonstrate that the selective pressures for organisms within a single water mass vary based on differences in generation timescales resulting in different evolutionary strategies being favored. Organisms that experience more variable environments should favor a low-γ strategy. Furthermore, faster cell division rates should be a key factor in genetic adaptation in a changing ocean. Understanding and quantifying the relationship between evolutionary and physical timescales is critical for robust predictions of future microbial dynamics.

Marine microbes form the base of ocean food webs and drive ocean biogeochemical cycling. Yet little is known about how microbial populations will evolve due to global change-driven shifts in ocean dynamics. Understanding adaptive timescales is critical where long-term trends (e.g. warming) are coupled to shorter-term advection dynamics that move organisms rapidly between ecoregions. Here we investigated the interplay between physical and biological timescales using a model of adaptation and an eddy-resolving ocean circulation climate model. Two criteria (α and β) were identified that relate physical and biological timescales and determine the timing and nature of adaptation. Genetic adaptation was impeded in highly variable regimes (α1). An evolutionary trade-off emerged where greater short-term transgenerational effects (low-β-strategy) enabled rapid responses to environmental fluctuations but delayed genetic adaptation, while fewer short-term transgenerational effects (high-β-strategy) allowed faster genetic adaptation but inhibited short-term responses. Our results suggest that organisms with faster growth rates are better positioned to adapt to rapidly changing ocean conditions and that more variable environments will favor a bet-hedging, low-β-strategy. Understanding the relationship between evolutionary and physical timescales is critical for robust predictions of future microbial dynamics.

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., Simons Foundation (Award 329108), Gordon and Betty Moore Foundation (Grant GBMF3778), National Science Foundation (U.S.) (Grant OCE-1315201), National Science Foundation (U.S.) (Grant OCE-1558702), National Science Foundation (U.S.) (Grant 1434007)