Diverse CO₂-Induced Responses in Physiology and Gene Expression among Eukaryotic Phytoplankton

With rising atmospheric CO₂, phytoplankton face shifts in ocean chemistry including increased dissolved CO₂ and acidification that will likely influence the relative competitive fitness of different phytoplankton taxa. Here we compared the physiological and gene expression responses of six species of phytoplankton including a diatom, a raphidophyte, two haptophytes, and two dinoflagellates to ambient (~400 ppm) and elevated (~800 ppm) CO₂. Dinoflagellates had significantly slower growth rates and higher, yet variable, chlorophyll a per cell under elevated CO₂. The other phytoplankton tended to have increased growth rates and/or decreased chlorophyll a per cell. Carbon and nitrogen partitioning of cells shifted under elevated CO₂ in some species, indicating potential changes in energy fluxes due to changes in carbon concentrating mechanisms (CCM) or photorespiration. Consistent with these phenotypic changes, gene set enrichment analyses revealed shifts in energy, carbon and nitrogen metabolic pathways, though with limited overlap between species in the genes and pathways involved. Similarly, gene expression responses across species revealed few conserved CO₂-responsive genes within CCM and photorespiration categories, and a survey of available transcriptomes found high diversity in biophysical CCM and photorespiration expressed gene complements between and within the four phyla represented by these species. The few genes that displayed similar responses to CO₂ across phyla were from understudied gene families, making them targets for further research to uncover the mechanisms of phytoplankton acclimation to elevated CO₂. These results underscore that eukaryotic phytoplankton have diverse gene complements and gene expression responses to CO₂ perturbations and highlight the value of cross-phyla comparisons for identifying gene families that respond to environmental change.