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Nitrification controls the oxidation state of bioavailable nitrogen. Distinct clades of chemoautotrophic microorganisms – predominantly ammonia-oxidizing archaea (AOA) and nitrite-oxidizing bacteria (NOB) – regulate the two steps of nitrification in the ocean, but explanations for their observed relative abundances and nitrification rates remain incomplete and their contributions to the global marine carbon cycle via carbon fixation remain unresolved. Using a mechanistic microbial ecosystem model with nitrifying functional types, we derive simple expressions for the controls on AOA and NOB in the deep, oxygenated open ocean. The relative biomass yields, loss rates, and cell quotas of AOA and NOB control their relative abundances, though we do not need to invoke a difference in loss rates to explain the observed relative abundances. The supply of ammonium, not the traits of AOA or NOB, controls the relatively equal ammonia and nitrite oxidation rates at steady state. The relative yields of AOA and NOB alone set their relative bulk carbon fixation rates in the water column. The quantitative relationships are consistent with multiple in situ datasets. In a complex global ecosystem model, nitrification emerges dynamically across diverse ocean environments, and ammonia and nitrite oxidation and their associated carbon fixation rates are decoupled due to physical transport and complex ecological interactions in some environments. Nevertheless, the simple expressions capture global patterns to first order. The model provides a mechanistic upper estimate on global chemoautotrophic carbon fixation of 0.2–0.5 Pg C yr−1, which is on the low end of the wide range of previous estimates. Modeled carbon fixation by AOA (0.2–0.3 Pg C yr−1) exceeds that of NOB (about 0.1 Pg C yr−1) because of the higher biomass yield of AOA. The simple expressions derived here can be used to quantify the biogeochemical impacts of additional metabolic pathways (i.e., mixotrophy) of nitrifying clades and to identify alternative metabolisms fueling carbon fixation in the deep ocean.

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, Marine microbial activities fuel biogeochemical cycles that impact the climate, but global models do not account for the myriad physiological processes that microbes perform. Here the authors argue for a model framework that reinterprets the ocean as physics coupled to biologically-driven redox chemistry.

Sinking particulate organic carbon out of the surface ocean sequesters carbon on decadal to millennial timescales. Predicting the particulate carbon flux is therefore critical for understanding both global carbon cycling and the future climate. Microbes play a crucial role in particulate organic carbon degradation, but the impact of depth-dependent microbial dynamics on ocean-scale particulate carbon fluxes is poorly understood. Here we scale-up essential features of particle-associated microbial dynamics to understand the large-scale vertical carbon flux in the ocean. Our model provides mechanistic insight into the microbial contribution to the particulate organic carbon flux profile. We show that the enhanced transfer of carbon to depth can result from populations struggling to establish colonies on sinking particles due to diffusive nutrient loss, cell detachment, and mortality. These dynamics are controlled by the interaction between multiple biotic and abiotic factors. Accurately capturing particle-microbe interactions is essential for predicting variability in large-scale carbon cycling.

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 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., Organic matter constitutes a key reservoir in global elemental cycles. However, our understanding of the dynamics of organic matter and its accumulation remains incomplete. Seemingly disparate hypotheses have been proposed to explain organic matter accumulation: the slow degradation of intrinsically recalcitrant substrates, the depletion to concentrations that inhibit microbial consumption, and a dependency on the consumption capabilities of nearby microbial populations. Here, using a mechanistic model, we develop a theoretical framework that explains how organic matter predictably accumulates in natural environments due to biochemical, ecological, and environmental factors. Our framework subsumes the previous hypotheses. Changes in the microbial community or the environment can move a class of organic matter from a state of functional recalcitrance to a state of depletion by microbial consumers. The model explains the vertical profile of dissolved organic carbon in the ocean and connects microbial activity at subannual timescales to organic matter turnover at millennial timescales. The threshold behavior of the model implies that organic matter accumulation may respond nonlinearly to changes in temperature and other factors, providing hypotheses for the observed correlations between organic carbon reservoirs and temperature in past earth climates.

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.

Methylmercury is greatly bioconcentrated and biomagnified in marine plankton ecosystems, and these communities form the basis of marine food webs. Therefore, evaluating the potential exposure of methylmercury to higher trophic levels, including humans, requires a better understanding of its distribution in the ocean and the factors that control its biomagnification. In this study, a coupled physical/ecological model was used to simulate the trophic transfer of monomethylmercury (MMHg) in a marine plankton ecosystem. The model includes phytoplankton, a microbial community, herbivorous zooplankton (HZ), and carnivorous zooplankton (CZ). The model captured both shorter food chains in oligotrophic regions, with small HZ feeding on small phytoplankton, and longer chains in higher nutrient conditions, with larger HZ feeding on larger phytoplankton and larger CZ feeding on larger HZ. In the model, trophic dilution occurred in the food webs that involved small zooplankton, as the grazing fluxes of small zooplankton were insufficient to accumulate more MMHg in themselves than in their prey. The model suggested that biomagnification was more prominent in large zooplankton and that the microbial community played an important role in the trophic transfer of MMHg. Sensitivity analyses showed that with increasing body size, the sensitivity of the trophic magnification ratio to grazing, mortality rates, and food assimilation efficiency (AEC) increased, while the sensitivity to excretion rates decreased. More predation or a longer zooplankton lifespan may lead to more prominent biomagnification, especially for large species. Because lower AEC resulted in more predation, modeled ratios of MMHg concentrations between large CZ and HZ doubled when the AEC decreased from 40% to 10%. This suggested that the biomagnification of large zooplankton was particularly sensitive to food assimilation efficiency.

Remineralization of organic matter by heterotrophic organisms regulates the biological sequestration of carbon, thereby mediating atmospheric CO2. While surface nutrient supply impacts the elemental ratios of primary production, stoichiometric control by remineralization remains unclear. Here we develop a mechanistic description of remineralization and its stoichiometry in a marine microbial ecosystem model. The model simulates the observed elemental plasticity of phytoplankton and the relatively constant, lower C:N of heterotrophic biomass. In addition, the model captures the observed decreases in DOC:DON and the C:N remineralization ratio with depth for more labile substrates, which are driven by a switch in the dominant source of labile DOM from phytoplankton to heterotrophic biomass. Only a model version with targeted remineralization of N-rich components is able to simulate the observed profiles of preferential remineralization of DON relative to DOC and the elevated C:N of bulk DOM. The model suggests that more labile substrates are associated with C-limited heterotrophic growth and not with preferential remineralization, while more recalcitrant substrates are associated with growth limited by processing rates and with preferential remineralization. The resulting patterns of variable remineralization stoichiometry mediate the extent to which a proportional increase in carbon production resulting from changes in phytoplankton stoichiometry can increase the efficiency of the biological pump. Results emphasize the importance of understanding the physiology of both phytoplankton and heterotrophs for anticipating changes in biologically driven ocean carbon storage.

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)

Limnology and Oceanography published by Wiley Periodicals, Inc. on behalf of Association for the Sciences of Limnology and Oceanography When aerobic microbes deplete oxygen sufficiently, anaerobic metabolisms activate, driving losses of fixed nitrogen from marine oxygen minimum zones. Biogeochemical models commonly prescribe a 1–10 μM critical oxygen concentration for this transition, a range consistent with previous empirical and recent theoretical work. However, the recently developed STOX sensor has revealed large regions with much lower oxygen concentrations, at or below its 1–10 nM detection limit. Here, we develop a simplified metabolic model of an aerobic microbe to provide a theoretical interpretation of this observed depletion. We frame the threshold as O*2, the subsistence oxygen concentration of an aerobic microbial metabolism, at which anaerobic metabolisms can coexist with or outcompete aerobic growth. The framework predicts that this minimum oxygen concentration varies with environmental and physiological factors and is in the nanomolar range for most marine environments, consistent with observed concentrations. Using observed grazing rates to calibrate the model, we predict a minimum oxygen concentration of order 0.1–10 nM in the core of a coastal anoxic zone. We also present an argument for why anammox may be energetically favorable at a higher oxygen concentration than denitrification, as some observations suggest. The model generates hypotheses that could be tested in the field and provides a simple, mechanistic, and dynamic parameterization of oxygen depletion for biogeochemical models, without prescription of a fixed critical oxygen concentration., Gordon and Betty Moore Foundation (Grant GBMF3778), Simons Foundation (Grant P49480), United States. National Aeronautics and Space Administration (Grant NNX13AC34G), National Science Foundation (U.S.) (Grant OCE-1259388)