Nutrient limitation increases CO2-dependent sensitivity of C-isotopic fractionation in Protoceratium reticulatum
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Stable carbon isotope fractionation (εp) of marine phytoplankton is influenced by aqueous carbon dioxide concentrations ([CO2(aq)]), cell morphology and metabolic pathways, which can further be influenced by environmental parameters, such as nutrient limitation. Increases in pCO2 levels, and duo-limitation of nitrogen (N) and phosphorus (P) from strengthening of ocean stratification, are two of the predicted consequences of a changing climate due to anthropogenic fossil fuel consumption. In this study, we investigate Protoceratum reticulatum, an ecologically, economically and palaeo-environmentally significant yessotoxin-producing dinoflagellate, under representations of past (180 µatm), modern (400 µatm) and projected (1000 µatm) pCO2 levels, in combination with limitation of essential nutrients N and P. Growth responses, internal stoichiometry, toxin production, and εpwere all analysed for singular effects of nutrient and pCO2, as well as the interaction between treatments. Toxin contents were independent of pCO2 under nutrient replete treatments, but showed a negative correlation with pCO2 under nutrient limitation. Highest toxin contents were found under nutrient limiting conditions at the lowest pCO2 . Growth rates(µ) remained independent of nutrient limitation, and all growth response parameters (growth rate and population biovolume) were optimised around present day levels. PON and POP quota and production all decreased under nutrient limitation, and more so for the low CO2 treatments. All nutrient ratios increased significantly with nutrient limitation, and caused deviations to the constant intracellular elemental stoichiometry that was otherwise maintained under nutrient replete treatments. POC quota and production, despite increasing under nutrient limtitation, maintained a constant relationship with stable carbon isotope fractionation for both nutrient treatments. εp remained strongly CO2-dependent for both nutrient treatments,with significant increases in εp values observed under nutrient limitation. CO2-dependent sensitivity of εp also increased under nutrient limitation, indicating potential changes in carbon species use and/or possible changes related to leakage. We found εp to be largely unaffected by µ, but largely influenced by POC content and pCO2, and indirectly influenced by nutrient limitation, which could suggest changes in CCM mode or decrease in CCM functioning under nutrient limiting conditions. The potential increase in carbon fixation under nutrient limited conditions at high levels of pCO2, in conjuction with increased intracellular carbon contents and changes in internal stoichiometry are likely to impact on oceanic carbon cycling of the biological pump, potentially altering the ocean’s capacity to buffer carbon. The strong CO2-dependency of 13C fractionation, even at low pCO2 levels, indicates a predominant diffusive uptake of CO2 by P. reticulatum under both nutrient replete and nutrient limiting conditions. This, along with the increased CO2-dependent sensitivity of εp under nutrient limiting conditions, provides potential for use of P. reticulatum in the running for a fossilized dinoflagellate CO2 proxy. However, additional experiments should test for strain-specific inorganic carbon uptake mechanisms, as well as directly testing possible offsets that might occur for 13C values between cells and cysts.