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ABSTRACT Photoautotrophic diazotrophs, specifically the generaTrichodesmiumand UCYN-A, play a pivotal role in marine nitrogen cycling through their capacity for nitrogen fixation. Despite their global distribution, the microdiversity and environmental drivers of these diazotrophs remain underexplored. This study provides a comprehensive analysis of the global diversity and distribution ofTrichodesmiumand UCYN-A using the nitrogenase gene (nifH) as a genetic marker. We sequenced 954 samples from the Pacific, Atlantic, and Indian Oceans as part of the Bio-GO-SHIP project. Our results reveal significant phylogenetic and biogeographic differences between and within the two genera.Trichodesmiumexhibited greater microdiversity compared to UCYN-A, with clades showing region-specific distribution.Trichodesmiumclades were primarily influenced by temperature and nutrient availability. They were particularly frequent in regions of phosphorus stress. In contrast, UCYN-A was most frequently observed in regions experiencing iron stress. UCYN-A clades demonstrated more homogeneous distributions, with a single sequence variant within the UCYN-A1 clade dominating across varied environments. The biogeographic patterns and environmental correlations ofTrichodesmiumand UCYN-A highlight the role of microdiversity in their ecological adaptation and reflect their different ecological strategies. These findings underscore the importance of characterizing the global patterns of fine-scale genetic diversity to better understand the functional roles and distribution of marine nitrogen-fixing photoautotrophs.IMPORTANCEThis study provides insights into the global diversity and distribution of nitrogen-fixing photoautotrophs, specificallyTrichodesmiumand UCYN-A. We sequenced 954 oceanic samples of thenifHnitrogenase gene and uncovered significant differences in microdiversity and environmental associations between these genera.Trichodesmiumshowed high levels of sequence diversity and region-specific clades influenced by temperature and nutrient availability. In contrast, UCYN-A exhibited a more uniform distribution, thriving in iron-stressed regions. Quantifying these fine-scale genetic variations enhances our knowledge of their ecological roles and adaptations, emphasizing the need to characterize the genetic diversity of marine nitrogen-fixing prokaryotes. 

Abstract Oceanic nutrient cycles are coupled, yet carbon-nitrogen-phosphorus (C:N:P) stoichiometry in marine ecosystems is variable through space and time, with no clear consensus on the controls on variability. Here, we analyze hydrographic, plankton genomic diversity, and particulate organic matter data from 1970 stations sampled during a global ocean observation program (Bio-GO-SHIP) to investigate the biogeography of surface ocean particulate organic matter stoichiometry. We find latitudinal variability in C:N:P stoichiometry, with surface temperature and macronutrient availability as strong predictors of stoichiometry at high latitudes. Genomic observations indicated community nutrient stress and suggested that nutrient supply rate and nitrogen-versus-phosphorus stress are predictive of hemispheric and regional variations in stoichiometry. Our data-derived statistical model suggests that C:P and N:P ratios will increase at high latitudes in the future, however, changes at low latitudes are uncertain. Our findings suggest systematic regulation of elemental stoichiometry among ocean ecosystems, but that future changes remain highly uncertain. 

Abstract A key uncertainty for predicting future ocean oxygen levels is the response and feedback of organic matter respiration demand. One poorly constrained component of the respiration demand is the oxygen‐to‐carbon remineralization ratio—the respiration quotient. Currently, multiple biological hypotheses can explain variation in the respiration quotient of organic matter produced in the surface ocean. To test these hypotheses, we directly quantified the particulate respiration quotient in 715 samples along a meridional section of the Atlantic Ocean and compared to previous Pacific Ocean observations. We demonstrate significant regional shifts in the respiration quotient and a two‐basin average of 1.16. Possible diel oscillations were also observed in the respiration quotient. Basin and regional variation in the respiration quotient were positively linked to temperature, N versus P stress, and plankton size structure. These observations suggest a complex regulation of the respiration quotient with important implications for the regional coupling of carbon and oxygen cycling. 

Abstract Detailed descriptions of microbial communities have lagged far behind physical and chemical measurements in the marine environment. Here, we present 971 globally distributed surface ocean metagenomes collected at high spatio-temporal resolution. Our low-cost metagenomic sequencing protocol produced 3.65 terabases of data, where the median number of base pairs per sample was 3.41 billion. The median distance between sampling stations was 26 km. The metagenomic libraries described here were collected as a part of a biological initiative for the Global Ocean Ship-based Hydrographic Investigations Program, or “Bio-GO-SHIP.” One of the primary aims of GO-SHIP is to produce high spatial and vertical resolution measurements of key state variables to directly quantify climate change impacts on ocean environments. By similarly collecting marine metagenomes at high spatiotemporal resolution, we expect that this dataset will help answer questions about the link between microbial communities and biogeochemical fluxes in a changing ocean. 

Abstract Environmentally driven variability in the elemental stoichiometry of ocean plankton plays a key role in ocean biogeochemical processes. Recent studies have identified clear regional variability in C:N:P, but less is known about the environmental regulation of diel variability in plankton elemental stoichiometry. Here, we quantified the amplitude of the diel variability in C:N of surface ocean particles (<30 μm,C:N_amp) across large latitudinal gradients in the Indian and Atlantic Oceans. We commonly observed diel oscillations in C:N and biome‐specific variability inC:N_amp. Temperature emerged as the strongest predictor ofC:N_amp, relative to the supply of nitrate. We propose thatC:N_ampis positively related to photosynthesis and respiration and thus phytoplankton growth rates. We find that independent growth rate proxies and an ecosystem model support this hypothesis. In addition, the temperature sensitivity ofC:N_amphas aQ₁₀of 1.78 corroborating studies of phytoplankton growth rates. Surface communities across the Indian Ocean transect had a very small dependency on nitrate, whereas recycled nitrogen sources were by far the most preferred and the ratio of recycled‐N:nitrate utilization increased with increasingC:N_amp. To predict future changes inC:N_amp, we combined our statistical model with data from the fifth Coupled Model Intercomparison Project for the years 1990 and 2090. The results suggest that future rising temperatures will yield increasedC:N_amp. Collectively, our results imply that rising surface ocean temperatures lead to elevated phytoplankton growth rates supported by recycled nutrients. 

Abstract Climate change is projected to modify the physical and chemical environment of the ocean, but the quantitative impact on the distribution of phytoplankton groups is unclear. Most Earth System Models (ESMs) predict future declines of phytoplankton in low latitude waters, contradicting observations showing that picophytoplankton can reach high abundance in warm waters. Here, we used a historic and three climate scenarios along with quantitative niche models to projectProchlorococcus,Synechococcus, and picoeukaryotic phytoplankton distributions for the year 2100. First, we found global responses with up to 50% and 9% increase forProchlorococcusandSynechococcusabundances, respectively, and 8% decrease for picoeukaryotic phytoplankton. All groups increased in abundance at low latitude, andSynechococcusand picoeukaryotic phytoplankton showed bands of decreases and increases in mid‐ and high‐latitudes, respectively.Prochlorococcustemporal trends were consistent among ESMs and increased with the strength of the scenario, whileSynechococcusand picoeukaryotic phytoplankton showed mixed results. Second, we evaluated sources of uncertainty associated to future projections. The anthropogenic uncertainty, associated to climate scenarios, increased with time and was relevant forProchlorococcus. The environmental and biological uncertainty, associated to ESMs and niche models, respectively, represented the largest fraction but differed among lineages. Quantifying uncertainties is key because the predicted differences in the future distribution and abundance can have large‐scale consequences on ocean ecosystem functioning. 

Abstract Are the oceans turning into deserts? Rising temperature, increasing surface stratification, and decreasing vertical inputs of nutrients are expected to cause an expansion of warm, nutrient deplete ecosystems. Such an expansion is predicted to negatively affect a trio of key ocean biogeochemical features: phytoplankton biomass, primary productivity, and carbon export. However, phytoplankton communities are complex adaptive systems with immense diversity that could render them at least partially resilient to global changes. This can be illustrated by the biology of theProchlorococcus“collective.” Adaptations to counter stress, use of alternative nutrient sources, and frugal resource allocation can allowProchlorococcusto buffer climate‐driven changes in nutrient availability. In contrast, cell physiology is more sensitive to temperature changes. Here, we argue that biogeochemical models need to consider the adaptive potential of diverse phytoplankton communities. However, a full understanding of phytoplankton resilience to future ocean changes is hampered by a lack of global biogeographic observations to test theories. We propose that the resilience may in fact be greater in oligotrophic waters than currently considered with implications for future predictions of phytoplankton biomass, primary productivity, and carbon export. 

Abstract Concentrations and elemental stoichiometry of suspended particulate organic carbon, nitrogen, phosphorus, and oxygen demand for respiration (C:N:P:−O 2 ) play a vital role in characterizing and quantifying marine elemental cycles. Here, we present Version 2 of the Global Ocean Particulate Organic Phosphorus, Carbon, Oxygen for Respiration, and Nitrogen (GO-POPCORN) dataset. Version 1 is a previously published dataset of particulate organic matter from 70 different studies between 1971 and 2010, while Version 2 is comprised of data collected from recent cruises between 2011 and 2020. The combined GO-POPCORN dataset contains 2673 paired surface POC/N/P measurements from 70°S to 73°N across all major ocean basins at high spatial resolution. Version 2 also includes 965 measurements of oxygen demand for organic carbon respiration. This new dataset can help validate and calibrate the next generation of global ocean biogeochemical models with flexible elemental stoichiometry. We expect that incorporating variable C:N:P:-O 2 into models will help improve our estimates of key ocean biogeochemical fluxes such as carbon export, nitrogen fixation, and organic matter remineralization. 

In this article, we present Bio-GO-SHIP, a new ocean observing program that will incorporate sustained and consistent global biological ocean observations into the Global Ocean Ship-based Hydrographic Investigations Program (GO-SHIP). The goal of Bio-GO-SHIP is to produce systematic and consistent biological observations during global ocean repeat hydrographic surveys, with a particular focus on the planktonic ecosystem. Ocean plankton are an essential component of the earth climate system, form the base of the oceanic food web and thereby play an important role in influencing food security and contributing to the Blue Economy. Despite its importance, ocean biology is largely under-sampled in time and space compared to physical and chemical properties. This lack of information hampers our ability to understand the role of plankton in regulating biogeochemical processes and fueling higher trophic levels, now and in future ocean conditions. Traditionally, many of the methods used to quantify biological and ecosystem essential ocean variables (EOVs), measures that provide valuable information on the ecosystem, have been expensive and labor- and time-intensive, limiting their large-scale deployment. In the last two decades, new technologies have been developed and matured, making it possible to greatly expand our biological ocean observing capacity. These technologies, including cell imaging, bio-optical sensors and 'omic tools, can be combined to provide overlapping measurements of key biological and ecosystem EOVs. New developments in data management and open sharing can facilitate meaningful synthesis and integration with concurrent physical and chemical data. Here we outline how Bio-GO-SHIP leverages these technological advances to greatly expand our knowledge and understanding of the constituents and function of the global ocean plankton ecosystem. 

Nutrient supply regulates the activity of phytoplankton, but the global biogeography of nutrient limitation and co-limitation is poorly understood.Prochlorococcusadapt to local environments by gene gains and losses, and we used genomic changes as an indicator of adaptation to nutrient stress. We collected metagenomes from all major ocean regions as part of the Global Ocean Ship-based Hydrographic Investigations Program (Bio-GO-SHIP) and quantified shifts in genes involved in nitrogen, phosphorus, and iron assimilation. We found regional transitions in stress type and severity as well as widespread co-stress.Prochlorococcusstress genes, bottle experiments, and Earth system model predictions were correlated. We propose that the biogeography of multinutrient stress is stoichiometrically linked by controls on nitrogen fixation. Our omics-based description of phytoplankton resource use provides a nuanced and highly resolved description of nutrient stress in the global ocean.