The Role of Ocean Currents in the Temperature Selection of Plankton: Insights from an Individual-Based Model.

Biogeography studies that correlate the observed distribution of organisms to environmental variables are typically based on local conditions. However, in cases with substantial translocation, like planktonic organisms carried by ocean currents, selection may happen upstream and local environmental factors may not be representative of those that shaped the local population. Here we use an individual-based model of microbes in the global surface ocean to explore this effect for temperature. We simulate up to 25 million individual cells belonging to up to 50 species with different temperature optima. Microbes are moved around the globe based on a hydrodynamic model, and grow and die based on local temperature. We quantify the role of currents using the "advective temperature differential" metric, which is the optimum temperature of the most abundant species from the model with advection minus that from the model without advection. This differential depends on the location and can be up to 4°C. Poleward-flowing currents, like the Gulf Stream, generally experience cooling and the differential is positive. We apply our results to three global datasets. For observations of optimum growth temperature of phytoplankton, accounting for the effect of currents leads to a slightly better agreement with observations, but there is large variability and the improvement is not statistically significant. For observed Prochlorococcus ecotype ratios and metagenome nucleotide divergence, accounting for advection improves the correlation significantly, especially in areas with relatively strong poleward or equatorward currents.

Interactions between Thermal Acclimation, Growth Rate, and Phylogeny Influence Prochlorococcus Elemental Stoichiometry.

Variability in plankton elemental requirements can be important for global ocean biogeochemistry but we currently have a limited understanding of how ocean temperature influences the plankton C/N/P ratio. Multiple studies have put forward a 'translation-compensation' hypothesis to describe the positive relationship between temperature and plankton N/P or C/P as cells should have lower demand for P-rich ribosomes and associated depressed QP when growing at higher temperature. However, temperature affects many cellular processes beyond translation with unknown outcomes on cellular elemental composition. In addition, the impact of temperature on growth and elemental composition of phytoplankton is likely modulated by the life history and growth rate of the organism. To test the direct and indirect (via growth rate changes) effect of temperature, we here analyzed the elemental composition and ratios in six strains affiliated with the globally abundant marine Cyanobacteria Prochlorococcus. We found that temperature had a significant positive effect on the carbon and nitrogen cell quota, whereas no clear trend was observed for the phosphorus cell quota. The effect on N/P and C/P were marginally significantly positive across Prochlorococcus. The elemental composition and ratios of individual strains were also affected but we found complex interactions between the strain identity, temperature, and growth rate in controlling the individual elemental ratios in Prochlorococcus and no common trends emerged. Thus, the observations presented here does not support the 'translation-compensation' theory and instead suggest unique cellular elemental effects as a result of rising temperature among closely related phytoplankton lineages. Thus, the biodiversity context should be considered when predicting future elemental ratios and how cycles of carbon, nitrogen, and phosphorus may change in a future ocean.

Variable but persistent coexistence of Prochlorococcus ecotypes along temperature gradients in the ocean's surface mixed layer.

The vast majority of the phytoplankton communities in surface mixed layer of the oligotrophic ocean are numerically dominated by one of two ecotypes of Prochlorococcus, eMIT9312 or eMED4. In this study, we surveyed large latitudinal transects in the Atlantic and Pacific Ocean to determine if these ecotypes discretely partition the surface mixed layer niche, or if populations exist as a continuum along key environmental gradients, particularly temperature. Transitions of dominance occurred at approximately 19-21°C, with the eMED4 ecotype dominating the colder, and eMIT9312 ecotype dominating the warmer regions. Within these zones of regional dominance, however, the minority ecotype was not competed to extinction. Rather, a robust log-linear relationship between ecotype ratio and temperature characterized this stabilized coexistence: for every 2.5°C increase in temperature, the eMIT9312:eMED4 ratio increased by an order of magnitude. This relationship was observed in both quantitative polymerase chain reaction and in pyrosequencing assays. Water column stratification also contributed to the ecotype ratio along the basin-scale transects, but to a lesser extent. Finally, instances where the ratio of the eMED4 and eMIT9312 abundances did not correlate well with temperature were identified. Such occurrences are likely due to changes in water temperatures outpacing changes in community structure.

In situ activity of a dominant Prochlorococcus ecotype (eHL-II) from rRNA content and cell size.

In the open ocean genetically diverse clades of the unicellular cyanobacteria Prochlorococcus are biogeographically structured along environmental gradients, yet little is known about their in situ activity. To address this gap, here we use the numerically dominant Prochlorococcus clade eHL-II (eMIT9312) as a model organism to develop and apply a method to examine their in situ activity using rRNA content and cell size as metrics of cellular physiology. For two representative isolates (MIT9312 and MIT9215) rRNA cell(-1) increases linearly with specific growth rate but is anticorrelated with cell size indicated by flow cytometrically measured (SSC). Although each strain has a unique relationship between cellular rRNA (or cell size) and growth rate, both strains have the same strong positive correlation between rRNA cell(-1) SSC(-1) and growth rate. We field test this approach and observe distinct patterns of eHL-II clade specific activity (rRNA cell(-1) SSC(-1)) with depth that are consistent with patterns of photosynthetic rates. This molecular technique provides unique insight into the ecology of Prochlorococcus and could potentially be expanded to include other microbes to unravel the ecological and biogeochemical contributions of genetically distinct marine side scatter microbes.