Intracellular pH regulation: characterization and functional investigation of H+ transporters in Stylophora pistillata

Abstract

Background Reef-building corals regularly experience changes in intra- and extracellular H+ concentrations ([H+]) due to physiological and environmental processes. Stringent control of [H+] is required to maintain the homeostatic acid-base balance in coral cells and is achieved through the regulation of intracellular pH (pHi). This task is especially challenging for reef-building corals that share an endosymbiotic relationship with photosynthetic dinoflagellates (family Symbiodinaceae), which significantly affect the pHi of coral cells. Despite their importance, the pH regulatory proteins involved in the homeostatic acid-base balance have been scarcely investigated in corals. Here, we report in the coral Stylophora pistillata a full characterization of the genomic structure, domain topology and phylogeny of three major H+ transporter families that are known to play a role in the intracellular pH regulation of animal cells; we investigated their tissue-specific expression patterns and assessed the effect of seawater acidification on their expression levels. Results We identified members of the Na+/H+ exchanger (SLC9), vacuolar-type electrogenic H+-ATP hydrolase (V-ATPase) and voltage-gated proton channel (HvCN) families in the genome and transcriptome of S. pistillata. In addition, we identified a novel member of the HvCN gene family in the cnidarian subclass Hexacorallia that has not been previously described in any species. We also identified key residues that contribute to H+ transporter substrate specificity, protein function and regulation. Last, we demonstrated that some of these proteins have different tissue expression patterns, and most are unaffected by exposure to seawater acidification. Conclusions In this study, we provide the first characterization of H+ transporters that might contribute to the homeostatic acid-base balance in coral cells. This work will enrich the knowledge of the basic aspects of coral biology and has important implications for our understanding of how corals regulate their intracellular environment.

Complex dynamics of coral gene expression responses to low pH across species

“…Corals tightly regulate intracellular pH via various transporters (Capasso et al., 2021). When comparing native origins, many genes related to calcium ion binding were differentially expressed in low pH conditions for both host P. astreoides and S. siderea .…”

“…Conversely, genes (3) related to voltage‐gated chloride or sodium activity were upregulated in host S. siderea Ojo versus Reef natives transplanted to a low pH environment, suggesting acclimatization to regulate chloride exchange/channel activity in Ojo natives living in low pH over longer time scales. Acid–base transport mechanisms, including transport proteins such as solute carrier (SLC) families, have an important role in intracellular pH regulation in corals (Capasso et al., 2021). Plasma membrane bicarbonate transporters, including SLC genes, are key to coral calcification (Zoccola et al., 2015).…”

The Impact of Symbiont Diversity on Cellular Integration and Function in the Cnidarian-Dinoflagellate Symbiosis

“…Proton transporters are central to pH homeostasis in corals (Capasso et al, 2021). VHA, a member of the P-type ATPase superfamily, is found in all domains of life (Chan et al, 2010).…”