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Establishing links between microbial diversity and environmental processes requires resolving the high degree of functional variation among closely related lineages or ecotypes. Here, we implement and validate an improved metagenomic approach that estimates the spatial biogeography and environmental regulation of ecotype-specific replication patterns (RObs) across ocean regions. A total of 719 metagenomes were analyzed from meridional Bio-GO-SHIP sections in the Atlantic and Indian Ocean. Accounting for sequencing bias and anchoring replication estimates in genome structure were critical for identifying physiologically relevant biological signals. For example, ecotypes within the dominant marine cyanobacteria Prochlorococcus exhibited distinct diel cycles in RObs that peaked between 19:00-22:00. Additionally, both Prochlorococcus ecotypes and ecotypes within the highly abundant heterotroph Pelagibacter (SAR11) demonstrated systematic biogeographies in RObs that differed from spatial patterns in relative abundance. Finally, RObs was significantly regulated by nutrient stress and temperature, and explained by differences in the genomic potential for nutrient transport, energy production, cell wall structure, and replication. Our results suggest that our new approach to estimating replication is reflective of gross population growth. Moreover, this work reveals that the interaction between adaptation and environmental change drives systematic variability in replication patterns across ocean basins that is ecotype-specific, adding an activity-based dimension to our understanding of microbial niche space.

Linking 'omics measurements with biogeochemical cycles is a widespread challenge in microbial community ecology. Here, we propose applying genomic adaptation as 'biosensors' for microbial investments to overcome nutrient stress. We then integrate this genomic information with a trait-based model to predict regional shifts in the elemental composition of marine plankton communities. We evaluated this approach using metagenomic and particulate organic matter samples from the Atlantic, Indian and Pacific Oceans. We find that our genome-based trait model significantly improves our prediction of particulate C : P (carbon : phosphorus) across ocean regions. Furthermore, we detect previously unrecognized ocean areas of iron, nitrogen and phosphorus stress. In many ecosystems, it can be very challenging to quantify microbial stress. Thus, a carefully calibrated genomic approach could become a widespread tool for understanding microbial responses to environmental changes and the biogeochemical outcomes. This article is part of the theme issue 'Conceptual challenges in microbial community ecology'.

The elemental ratios of carbon, nitrogen, and phosphorus (C:N:P) within organic matter play a key role in coupling biogeochemical cycles in the global ocean. At the cellular level, these ratios are controlled by physiological responses to the environment. But linking these cellular‐level processes to global biogeochemical cycles remains challenging. We present a novel model framework that combines knowledge of phytoplankton cellular functioning with global scale hydrographic data, to assess the role of variable carbon‐to‐phosphorus ratios (RC:P) on the distribution of export production. We implement a trait‐based mechanistic model of phytoplankton growth into a global biogeochemical inverse model to predict global patterns of phytoplankton physiology and stoichiometry that are consistent with both biological growth mechanisms and hydrographic carbon and nutrient observations. We compare this model to empirical parameterizations relating RC:P to temperature or phosphate concentration. We find that the way the model represents variable stoichiometry affects the magnitude and spatial pattern of carbon export, with globally integrated fluxes varying by up to 10% (1.3 Pg C yr−1) across models. Despite these differences, all models exhibit strong consistency with observed dissolved inorganic carbon and phosphate concentrations (R2 > 0.9), underscoring the challenge of selecting the most accurate model structure. We also find that the choice of parameterization impacts the capacity of changing RC:P to buffer predicted export declines. Our novel framework offers a pathway by which additional biological information might be used to reduce the structural uncertainty in model representations of phytoplankton stoichiometry, potentially improving our capacity to project future changes. Plain Language Summary: Phytoplankton play a vital role in Earth's carbon cycle. The ratios of carbon, nitrogen, and phosphorus in these tiny marine plants influence how much carbon they absorb at the surface and export to the deep ocean. Yet, many models overlook the global variability of these ratios. Our study introduces an innovative model that combines microscopic knowledge of phytoplankton growth with global ocean data. We use this model to predict how the elemental ratios in phytoplankton vary on a global scale. By comparing this detailed model to simpler models based on individual environmental controls, we reveal that the way we represent these ratios significantly impacts carbon export patterns. Different representations of these ratios lead to estimates of carbon export from the ocean's surface that differ by over 1 billion tons annually. We also find that the flexibility of elemental ratios can counteract future declines in ocean productivity to varying degrees, depending on the assumed environmental controls of these ratios. Our findings highlight the critical role of understanding the connection between phytoplankton elemental composition and their environment and underscore the need for improved models to better anticipate future changes in the ocean's carbon cycle. Key Points: New framework embeds a mechanistic cellular growth model for phytoplankton stoichiometry in a global biogeochemical inverse modelFour parameterizations of phytoplankton C:P ratios are optimized globally using an inverse model and multiple biogeochemical tracersModeled C:P patterns impact global carbon export flux by 10%, with larger regional differences, and affect sensitivity to future change [ABSTRACT FROM AUTHOR]

Marine phytoplankton stoichiometry links nutrient supply to marine carbon export. Deviations of phytoplankton stoichiometry from Redfield proportions (106C : 1P) could therefore have a significant impact on carbon cycling, and understanding which environmental factors drive these deviations may reveal new mechanisms regulating the carbon cycle. To explore the links between environmental conditions, stoichiometry, and carbon cycling, we compared four different models of phytoplankton C: P: a fixed Redfield model, a model with C: P given as a function of surface phosphorus concentration (P), a model with C: P given as a function of temperature, and a new multi-environmental model that predicts C: P as a function of light, temperature, and P. These stoichiometric models were embedded into a fivebox ocean circulation model, which resolves the three major ocean biomes (high-latitude, subtropical gyres, and tropical upwelling regions). Contrary to the expectation of a monotonic relationship between surface nutrient drawdown and carbon export, we found that lateral nutrient transport from lower C: P tropical waters to high C: P subtropical waters could cause carbon export to decrease with increased tropical nutrient utilization. It has been hypothesized that a positive feedback between temperature and pCO2,atm will play an important role in anthropogenic climate change, with changes in the biological pump playing at most a secondary role. Here we show that environmentally driven shifts in stoichiometry make the biological pump more influential, and may reverse the expected positive relationship between temperature and pCO2,atm. In the temperature-only model, changes in tropical temperature have more impact on the Δ pCO2,atm (~41 ppm) compared to subtropical temperature changes (~4.5 ppm). Our multi-environmental model predicted a decline in pCO2,atm of ~46 ppm when temperature spanned a change of 10 °C. Thus, we find that variation in marine phytoplankton stoichiometry and its environmental controlling factors can lead to nonlinear controls on pCO2,atm, suggesting the need for further studies of ocean C: P and the impact on ocean carbon cycling. [ABSTRACT FROM AUTHOR]

Marine phytoplankton stoichiometry links nutrient supply to marine carbon export. Deviations of phytoplankton stoichiometry from Redfield proportions (106C : 1P) could therefore have a significant impact on carbon cycling, and understanding which environmental factors drive these deviations may reveal new mechanisms that regulate the carbon cycle. To explore the links between environmental conditions, stoichiometry, and carbon cycling, we compared four different models for variations in phytoplankton C : P: a fixed Redfield model, a model with C : P given as a function of surface phosphorus concentration ([P]), a model with C : P given as a function of temperature, and a new multi-environmental model that predicts C : P as a function of light, temperature, and [P]. These stoichiometric models were embedded into a box model of the ocean circulation, which resolves the three major ocean biomes (high-latitude, subtropical gyres, and iron-limited tropical upwelling regions). Contrary to the expectation of a monotonic relationship between surface nutrient drawdown and carbon export, we found that lateral nutrient transport from lower C : P tropical waters to high C : P subtropical waters could cause carbon-export to decrease with increased tropical nutrient utilization. Temperature is thought to be one of the primary drivers of changes in atmospheric pCO2 (pCO2,atm) across glacial/interglacial periods, and it has been hypothesized that a positive feedback between temperature and pCO2,atm will play an important role in anthropogenic climate change, with changes in the biological pump playing at most a secondary role. Here we show that environmentally driven shifts in stoichiometry make the biological pump more influential, and may reverse the expected negative relationship between temperature and pCO2,atm. In the temperature-only model changes in tropical temperature have more impact on the Δ pCO2,atm (~ 41 ppm) compared to subtropical temperature (~ 4.5 ppm). Our multi-environmental model produced a decline in pCO2,atm of ~ 46 when temperature spanned a change of 10 °C. Thus, we find that variation in marine phytoplankton stoichiometry and its environmental controlling factor can lead to counterintuitive controls on pCO2,atm, suggesting the need for further studies of ocean C : P and the impact on ocean carbon cycling. [ABSTRACT FROM AUTHOR]