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Diverse phytoplankton modulate the coupling between the ocean carbon and nutrient cycles through life-history traits such as cell size, elemental quotas, and ratios. Biodiversity is mostly considered at broad functional levels, but major phytoplankton lineages are themselves highly diverse. As an example,Synechococcusis found in nearly all ocean regions, and we demonstrate contains extensive intraspecific variation. Here, we grew four closely relatedSynechococcusisolates in serially transferred cultures across a range of temperatures (16–25°C) to quantify for the relative role of intraspecific trait variation vs. environmental change. We report differences in cell size (p<0.01) as a function of strain and clade (p<0.01). The carbon (Q_C), nitrogen (Q_N), and phosphorus (Q_P) cell quotas all increased with cell size. Furthermore, cell size has an inverse relationship to growth rate. Within our experimental design, temperature alone had a weak physiological effect on cell quota and elemental ratios. Instead, we find systemic intraspecific variance of C:N:P, with cell size and N:P having an inverse relationship. Our results suggest a key role for intraspecific life history traits in determining elemental quotas and stoichiometry. Thus, the extensive biodiversity harbored within many lineages may modulate the impact of environmental change on ocean biogeochemical cycles. 

Abstract Recent studies have demonstrated regional differences in marine ecosystem C:N:P with implications for carbon and nutrient cycles. Due to strong co-variance, temperature and nutrient stress explain variability in C:N:P equally well. A reductionistic approach can link changes in individual environmental drivers with changes in biochemical traits and cell C:N:P. Thus, we quantified effects of temperature and nutrient stress on Synechococcus chemistry using laboratory chemostats, chemical analyses, and data-independent acquisition mass spectrometry proteomics. Nutrient supply accounted for most C:N:Pcell variability and induced tradeoffs between nutrient acquisition and ribosomal proteins. High temperature prompted heat-shock, whereas thermal effects via the “translation-compensation hypothesis” were only seen under P-stress. A Nonparametric Bayesian Local Clustering algorithm suggested that changes in lipopolysaccharides, peptidoglycans, and C-rich compatible solutes may also contribute to C:N:P regulation. Physiological responses match field-based trends in ecosystem stoichiometry and suggest a hierarchical environmental regulation of current and future ocean C:N:P. 

Abstract. Recent studies show that stoichiometric elemental ratios of marine ecosystems are not static at Redfield proportions but vary systematically between biomes. However, the wider Atlantic Ocean is undersampled for particulate organic matter (POM) elemental composition, especially when it comes to phosphorus (i.e., POP). Thus, it is uncertain how environmental variation in this region translates into shifts in the C:N:P ratio. To address this, we analyzed hydrography, genomics, and POM concentrations from 877 stations on the meridional transects AMT28 and C13.5, spanning the Atlantic Ocean. We observed nutrient-replete, high-latitude ecosystem C:N:P to be significantly lower than that in the oligotrophic gyres. Latitudinal and zonal differences in elemental stoichiometry were linked to overall nutrient supply as well as N vs. P stress. C:P and N:P were generally higher in the P-stressed northern region compared to Southern Hemisphere regions. We also detected a zonal difference linked to a westward deepening nutricline and a shift from N to P stress. We also evaluated possible seasonal changes in C:N:P across the basin and predicted these to be limited. Overall, this study confirms latitudinal shifts in surface ocean POM ratios but reveals previously unrecognized hemisphere and zonal gradients. This work demonstrates the importance of understanding how regional shifts in hydrography and type of nutrient stress shape the coupling between Atlantic Ocean nutrient and carbon cycles. 

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. 

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 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. 

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. 

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.