We examined the physiological responses of steady-state iron (Fe)-replete and Fe-limited cultures of the biogeochemically critical marine unicellular diazotrophic cyanobacterium Crocosphaera at glacial (19 Pa; 190 ppm), current (39 Pa; 380 ppm), and projected year 2100 (76 Pa; 750 ppm) CO 2 levels. Rates of N 2 and CO 2 fixation and growth increased in step with increasing partial pressure of CO 2 (pCO 2 ), but only under Fe-replete conditions. N 2 and carbon fixation rates at 75 Pa CO 2 were 1.4-1.8-fold and 1.2-2.0-fold higher, respectively, relative to those at present day and glacial pCO 2 levels. In Fe-replete cultures, cellular Fe and molybdenum quotas varied threefold and were linearly related to N 2 fixation rates and to external pCO 2 . However, N 2 fixation and trace metal quotas were decoupled from pCO 2 in Fe-limited Crocosphaera. Higher CO 2 and Fe concentrations both resulted in increased cellular pigment contents and affected photosynthesis vs. irradiance parameters. If these results also apply to natural Crocosphaera populations, anthropogenic CO 2 enrichment could substantially increase global oceanic N 2 and CO 2 fixation, but this effect may be tempered by Fe availability. Possible biogeochemical consequences may include elevated inputs of new nitrogen to the ocean and increased potential for Fe and/or phosphorus limitation in the future high-CO 2 ocean, and feedbacks to atmospheric pCO 2 in both the near future and over glacial to interglacial timescales.
The globally distributed colonial cyanobacterium Trichodesmium and unicellular diazotrophs including Crocosphaera together carry out the majority of marine biological nitrogen (N 2 ) fixation. Future sea surface warming is predicted to influence their abundance and distribution, but temperature reaction norms have been determined for very few representatives of each genus. We compared thermal responses within and between the 2 genera Trichodesmium and Crocosphaera by measuring reaction norms for growth, N 2 fixation, carbon fixation, and elemental ratios in 7 strains from a global culture collection. Temperature reaction norms of Trichodesmium and Crocosphaera were remarkably similar for all isolates within each genus, regardless of their geographic origin. Thermal limits of Trichodesmium and Crocosphaera ranged from 18 to 32°C and 24 to 32°C, and optimum growth temperatures were ~26 and ~30°C, respectively. The highest cellular ratios of nitrogen to phosphorus and carbon to nitrogen were found at optimum growth temperatures, and the lowest ratios near their thermal limits. In a mixed competition experiment, Trichodesmium growth rates were ~25% higher than those of Crocosphaera at 24°C, while those of Crocosphaera were ~50% higher at 28°C. Comparison of these results to current and projected seasonal temperature regimes in the subtropical Atlantic and Pacific Oceans suggests that predicted warmer temperatures may favor Crocosphaera over Trichodesmium, but that both genera may be excluded where future temperatures consistently exceed 32°C. Sea surface warming could profoundly alter the community structure and stoichiometry of marine N 2 -fixing cyanobacteria, thus fundamentally changing the biogeochemical cycling of this globally significant source of new nitrogen. Resale or republication not permitted without written consent of the publisher
Nutrient supply regulates the activity of phytoplankton, but the global biogeography of nutrient limitation and co-limitation is poorly understood. Prochlorococcus adapt 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. Prochlorococcus stress 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.
The factors that control elemental ratios within phytoplankton, like carbon:nitrogen:phosphorus (C:N:P), are key to biogeochemical cycles. Previous studies have identified relationships between nutrientlimited growth and elemental ratios in large eukaryotes, but little is known about these interactions in small marine phytoplankton like the globally important Cyanobacteria. To improve our understanding of these interactions in picophytoplankton, we asked how cellular elemental stoichiometry varies as a function of steady-state, N-and P-limited growth in laboratory chemostat cultures of Synechococcus WH8102. By combining empirical data and theoretical modeling, we identified a previously unrecognized factor (growth-dependent variability in cell size) that controls the relationship between nutrient-limited growth and cellular elemental stoichiometry. To predict the cellular elemental stoichiometry of phytoplankton, previous theoretical models rely on the traditional Droop model, which purports that the acquisition of a single limiting nutrient suffices to explain the relationship between a cellular nutrient quota and growth rate. Our study, however, indicates that growth-dependent changes in cell size have an important role in regulating cell nutrient quotas. This key ingredient, along with nutrient-uptake protein regulation, enables our model to predict the cellular elemental stoichiometry of Synechococcus across a range of nutrient-limited conditions. Our analysis also adds to the growth rate hypothesis, suggesting that P-rich biomolecules other than nucleic acids are important drivers of stoichiometric variability in Synechococcus. Lastly, by comparing our data with field observations, our study has important ecological relevance as it provides a framework for understanding and predicting elemental ratios in ocean regions where small phytoplankton like Synechococcus dominates.
Current hypotheses suggest that cellular elemental stoichiometry of marine eukaryotic phytoplankton such as the ratios of cellular carbon:nitrogen:phosphorus (C:N:P) vary between phylogenetic groups. To investigate how phylogenetic structure, cell volume, growth rate, and temperature interact to affect the cellular elemental stoichiometry of marine eukaryotic phytoplankton, we examined the C:N:P composition in 30 isolates across 7 classes of marine phytoplankton that were grown with a sufficient supply of nutrients and nitrate as the nitrogen source. The isolates covered a wide range in cell volume (5 orders of magnitude), growth rate (<0.01–0.9 d−1), and habitat temperature (2–24°C). Our analysis indicates that C:N:P is highly variable, with statistical model residuals accounting for over half of the total variance and no relationship between phylogeny and elemental stoichiometry. Furthermore, our data indicated that variability in C:P, N:P, and C:N within Bacillariophyceae (diatoms) was as high as that among all of the isolates that we examined. In addition, a linear statistical model identified a positive relationship between diatom cell volume and C:P and N:P. Among all of the isolates that we examined, the statistical model identified temperature as a significant factor, consistent with the temperature-dependent translation efficiency model, but temperature only explained 5% of the total statistical model variance. While some of our results support data from previous field studies, the high variability of elemental ratios within Bacillariophyceae contradicts previous work that suggests that this cosmopolitan group of microalgae has consistently low C:P and N:P ratios in comparison with other groups.
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