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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.

 

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.

 

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.

 

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. 

Ambient conditions shape microbiome responses to both short- and long-duration environment changes through processes including physiological acclimation, compositional shifts, and evolution. Thus, we predict that microbial communities inhabiting locations with larger diel, episodic, and annual variability in temperature and pH should be less sensitive to shifts in these climate-change factors. To test this hypothesis, we compared responses of surface ocean microbes from more variable (nearshore) and more constant (offshore) sites to short-term factorial warming (+3 °C) and/or acidification (pH −0.3). In all cases, warming alone significantly altered microbial community composition, while acidification had a minor influence. Compared with nearshore microbes, warmed offshore microbiomes exhibited larger changes in community composition, phylotype abundances, respiration rates, and metatranscriptomes, suggesting increased sensitivity of microbes from the less-variable environment. Moreover, while warming increased respiration rates, offshore metatranscriptomes yielded evidence of thermal stress responses in protein synthesis, heat shock proteins, and regulation. Future oceans with warmer waters may enhance overall metabolic and biogeochemical rates, but they will host altered microbial communities, especially in relatively thermally stable regions of the oceans.

 

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.

 

While the majority of studies use the environment to describe microbial populations, the high diversity of microbes can conversely be used as a resource to understand subtle environmental variability. Here, we used a high‐resolution spatial and temporal analysis ofProchlorococcussp. in the Eastern Indian Ocean to determine whether ecotypes and microdiverse taxa can be used to identify fine‐scale biogeochemical regimes in this under‐studied region. A total of 246 DNA samples were collected every 4–6 h in April 2016 on GO‐SHIP cruise I09N, which transected gyre, equatorial, and monsoonal ecosystems between Western Australia and the Bay of Bengal. Using amplicon sequencing of the highly variablerpoC1 marker, we found that the region was largely dominated by theProchlorococcusHL‐II clade. Conserved single nucleotide polymorphisms (SNPs) were used to identify four microdiverse haplotypes, or SNP‐delineated taxa, within the HL‐II clade ofProchlorococcus. The haplotypes showed regional patterns of relative gene count abundance that were significantly correlated with environmental conditions. Additionally, we used nonlinear least squares models to fit the sine wave function to our data and demonstrate that the haplotypes show distinct patterns in relative diel frequency, providing evidence that these microdiverse populations are ecologically and evolutionarily distinct. Overall, we show how the integration of a genomics data set into a biogeochemical framework can reveal a more nuanced understanding of a complex ocean basin.