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.
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Abstract 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.
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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.
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Abstract Concentrations and elemental ratios of suspended particulate organic matter influence many biogeochemical processes in the ocean, including patterns of phytoplankton nutrient limitation and links between carbon, nitrogen and phosphorus cycles. Here we present direct measurements of cellular nutrient content and stoichiometric ratios for discrete phytoplankton populations spanning broad environmental conditions across several ocean basins. Median cellular carbon-to-phosphorus and nitrogen-to-phosphorus ratios were positively correlated with vertical nitrate-to-phosphate flux for all phytoplankton groups and were consistently higher for cyanobacteria than eukaryotes. Light and temperature were inconsistent predictors of stoichiometric ratios. Across nutrient-rich and phosphorus-stressed biomes in the North Atlantic, but not in the nitrogen-stressed tropical North Pacific, we find that a combination of taxonomic composition and environmental acclimation best predict bulk particulate organic matter composition. Our findings demonstrate the central role of plankton biodiversity and plasticity in controlling linkages between ocean nutrient and carbon cycles in some regions.
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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 amp is 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 amp has aQ 10 of 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 Light penetration through the ocean creates underwater light color niches and photosynthetic organisms use specific strategies to capture light in these niches. The selection pressure for some cyanobacteria strains in the genus
Synechococcus that change color to absorb either blue or green light (chromatic acclimaters, or generalists) is not well understood. Here, we tested the hypothesis that changes in ocean spectra brought about by mixing preferentially selects for generalists within aSynechococcus population. We investigated ocean conditions that led to high proportions ofSynechococcus generalists versus specialists in a model ocean column, and compared simulations with in situ metagenomic and physical oceanographic data from major Bio‐GO‐SHIP cruises, supplemented with GEOTRACES and TARA Oceans, as well as the GOOS Argo Program and sea surface height from AVISO. We found that greater mixed layer depths selected for generalists in simulatedSynechococcus populations, but did not account for much of the variance in the partitioning of light‐harvesting strategies in situ. Rather, oceanographic signatures for upwelling areas and ocean fronts explained more of the variation betweenSynechococcus generalists and specialists in the ocean. Our results motivate further study of the in situ light environments of upwelling zones and ocean fronts, which are currently understudied as potential light‐driven niche habitats. -
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.
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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 project
Prochlorococcus ,Synechococcus , and picoeukaryotic phytoplankton distributions for the year 2100. First, we found global responses with up to 50% and 9% increase forProchlorococcus andSynechococcus abundances, respectively, and 8% decrease for picoeukaryotic phytoplankton. All groups increased in abundance at low latitude, andSynechococcus and picoeukaryotic phytoplankton showed bands of decreases and increases in mid‐ and high‐latitudes, respectively.Prochlorococcus temporal trends were consistent among ESMs and increased with the strength of the scenario, whileSynechococcus and 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 the
Prochlorococcus “collective.” Adaptations to counter stress, use of alternative nutrient sources, and frugal resource allocation can allowProchlorococcus to 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 Marine picophytoplankton is the most abundant photosynthetic group on Earth; however, it is still underrepresented in dynamic ecosystem models. Major constraints for understanding its role in the ecosystem at a global scale are sparse data and lack of a baseline description of its distribution. Here, we present three datasets to assess the global abundance of the principal groups of picophytoplankton,
Prochlorococcus ,Synechococcus , and picoeukaryotic phytoplankton: (1) a compilation of 109,045 field observations with ancillary environmental data, (2) a global monthly climatology of 1° grids from 0 to 200 m, and (3) four climate scenarios projections, from the Coupled Model Intercomparison Project 5, spanning years 1901 to 2100. Together this set of observational and modeled data can improve our understanding of the role of picophytoplankton in the global ecosystem.