Regulation of Carbon Metabolism by Environmental Conditions: A Perspective From Diatoms and Other Chromalveolates

Abstract

Diatoms belong to a major, diverse and species-rich eukaryotic clade, the Heterokonta, within the polyphyletic chromalveolates. They evolved as a result of secondary endosymbiosis with one or more Plantae ancestors, but their precise evolutionary history is enigmatic. Nevertheless, this has conferred them with unique structural and biochemical properties that have allowed them to flourish in a wide range of different environments and cope with highly variable conditions. We review the effect of pH, light and dark, and CO 2 concentration on the regulation of carbon uptake and assimilation. We discuss the regulation of the Calvin-Benson-Bassham cycle, glycolysis, lipid synthesis, and carbohydrate synthesis at the level of gene transcripts (transcriptomics), proteins (proteomics) and enzyme activity. In contrast to Viridiplantae where redox regulation of metabolic enzymes is important, it appears to be less common in diatoms, based on the current evidence, but regulation at the transcriptional level seems to be widespread. The role of post-translational modifications such as phosphorylation, glutathionylation, etc., and of protein-protein interactions, has been overlooked and should be investigated further. Diatoms and other chromalveolates are understudied compared to the Viridiplantae, especially given their ecological importance, but we believe that the ever-growing number of sequenced genomes combined with proteomics, metabolomics, enzyme measurements, and the application of novel techniques will provide a better understanding of how this important group of algae maintain their productivity under changing conditions.

A plastid antiporter as a bioindicator ofThalassiosira pseudonanaresilience

“…This is consistent with the expectation that seawater acidification will alter electrochemical gradients that govern pH gradients across membranes (Taylor et al, 2012). While diatoms typically maintain a neutral pH in the cytoplasm (Taylor et al, 2012;Goldman et al, 2017), the pH within the plastid is higher (pH ~8) during the light period, and decreases during the dark (pH ~7) (Launay et al, 2020). This pH homeostasis is essential for plastid function, and therefore, the expression dynamics of the antiporter captures the non-linear consequences of combined changes in multiple environmental factors that influence the overall physiological state of diatoms, making the antiporter a useful composite bioindicator of diatom resilience.…”

“…In particular, we have discovered a dramatic switch in the dynamical day/night expression patterns of a putative Na + (K + )/H + antiporter, which indicates a shift in diatom response to high CO2 conditions regardless of changes in other environmental conditions (e.g., PAR, UVR, nutrient limitation). Through GFP-tagging we determined that the putative antiporter is localized to the plastid membrane where it might function to help maintain an optimal pH for the activity of enzymes related to carbon fixation, photosynthesis, transport, and other metabolic processes (Launay et al, 2020). This is consistent with the expectation that seawater acidification will alter electrochemical gradients that govern pH gradients across membranes (Taylor et al, 2012).…”

“…During dark to light transitions, in many plants as well as diatoms, the internal pH of the plastid can increase from ~7 to ~8 (Colman and Rotatore, 1995), which is the optimal pH for the activity of most plastid enzymes, including RuBisCO and Calvin cycle enzymes (Goldman et al, 2017). Given that the cytosolic pH of diatoms in contemporary CO2 levels is in the range of 7.0 to 7.5 (Taylor et al, 2012;Höhner et al, 2016;Goldman et al, 2017;Launay et al, 2020), active efflux of H + or counter exchange of ions by means of antiporters may be necessary to achieve a pH of 8 inside the plastid. Studies on T. weissflogii have demonstrated that acidification of seawater proportionally decreases intracellular pH causing internal acidosis in diatoms (Goldman et al, 2017).…”

A new type of disordered CP12 protein in the marine diatom Thalassiosira pseudonana

“…The structural properties of CP12 from T. pseudonana, with putative dimeric coiled coil domain and disordered regions, suggest that it is not an alien as regard to other CP12s and might therefore have oneto-many functions. As the gene encoding this protein has also been found in other diatoms, it could be another facet of the enigmatic regulation of diatom metabolism [19,23,72]. These ndings extend the context for dynamic and coiled coil proteins related to their functions in photosynthesis regulation and stress in diatoms.…”

“…Little is known about CP12 in the diatoms, an ecologically important group of microalgae. Diatoms have a more complex evolutionary background than the other organisms mentioned above in which CP12 has been studied, and the regulation of their CBB enzymes is not fully understood [19]. The complex PRK-GAPDH-CP12 does not seem to be present [20][21][22][23] though there are some studies indicating a possible presence of CP12 in these organisms [20,24].…”