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

Abstract

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.

Response of Phytoplankton Assemblages From Naturally Acidic Coastal Ecosystems to Elevated pCO2

“…This also suggests that the Chl a per cell must have on average been higher under this treatment, to account for the lack of an effect on total Chl a concentrations, although we have no direct data at the cellular level for this. Increases in Chl a per cell in response to high pCO 2 have been previously reported in multiple dinoflagellates (e.g., Eberlein et al, 2016;Hennon et al, 2017). However, Chl a per cell in diatoms has been reported to increase modestly (Crawfurd et al, 2011) to stay the same (e.g., Hennon et al, 2017) or decrease (Jacob et al, 2017) under high pCO 2 .…”

“…Increases in Chl a per cell in response to high pCO 2 have been previously reported in multiple dinoflagellates (e.g., Eberlein et al, 2016;Hennon et al, 2017). However, Chl a per cell in diatoms has been reported to increase modestly (Crawfurd et al, 2011) to stay the same (e.g., Hennon et al, 2017) or decrease (Jacob et al, 2017) under high pCO 2 . Within the diatoms, the genera Skeletonema and Thalassiosira appeared to benefit more than others.…”

Multiple global change stressor effects on phytoplankton nutrient acquisition in a future ocean

“…Lastly, cell size is generally correlated with genome size [77,78], and processes such as adaptive gene loss and genomic streamlining may optimize nutrient acquisition traits in small phytoplankton species, particularly in more stable environments [79]. Conversely, it is conceivable that larger cells may have a greater gene redundancy, leading to more resilient traits [8], which may provide a competitive advantage in dynamic environments. In summary, the higher flexibility of larger phytoplankton species in response to direct and indirect effects of warming and elevated pCO 2 may, at least partially, offset their competitive disadvantage in nutrient acquisition.…”

“…(CCMs) [5][6][7][8]. Various studies, however, have shown that elevated pCO 2 does not necessarily enhance primary production, or may even have negative effects, e.g.…”

Inorganic carbon concentrating mechanisms in free‐living and symbiotic dinoflagellates and chromerids

“…The anion exchange inhibitor DIDS does not inhibit the pH drift, whose extent probably relates to HCO 3 À entry, in the marine Glenodinium foliaceum (Nimer et al 1997). SLC4 HCO 3 À transporters are known from the genomes of a species of the (present) Symbiodiniaceae (Aranda et al 2016), Alexandrium monilatum and Prorocentrum minimum (Hennon et al 2017) and Thoracosphaera heimii (Van de Waal et al 2013e Waal et al 2013; presumably these are expressed in the plasmalemma. The various SLC4 HCO 3 À transporters can be Na + :HCO 3 À symporters or HCO 3 À :Clantiporters; work on the dinoflagellate SLC4 is needed to determine the co-or counter-ions, and their stoichiometry (Liu et al 2015, Raven 2020, Raven and Beardall 2020, and hence the possibility that this transporter brings about active HCO 3 À influx with corresponding accumulation of HCO 3 À in the cytosol.…”