A Rhesus channel in the coral symbiosome membrane suggests a novel mechanism to regulate NH ₃ and CO ₂ delivery to algal symbionts

Abstract

Reef-building corals maintain an intracellular photosymbiotic association with dinoflagellate algae. As the algae are hosted inside the symbiosome, all metabolic exchanges must take place across the symbiosome membrane. Using functional studies in Xenopus oocytes, immunolocalization, and confocal Airyscan microscopy, we established that Acropora yongei Rh (ayRhp1) facilitates transmembrane NH 3 and CO 2 diffusion and that it is present in the symbiosome membrane. Furthermore, ayRhp1 abundance in the symbiosome membrane was highest around midday and lowest around midnight. We conclude that ayRhp1 mediates a symbiosomal NH 4 + -trapping mechanism that promotes nitrogen delivery to algae during the day—necessary to sustain photosynthesis—and restricts nitrogen delivery at night—to keep algae under nitrogen limitation. The role of ayRhp1-facilitated CO 2 diffusion is less clear, but it may have implications for metabolic dysregulation between symbiotic partners and bleaching. This previously unknown mechanism expands our understanding of symbioses at the immediate animal-microbe interface, the symbiosome.

Nitrogen competition is the general mechanism underlying cnidarian-Symbiodiniaceae symbioses

“…Such a mechanism might allow corals to mitigate some of the drawbacks resulting from their reduced ability to control their symbiont population. In line with this, a recent study suggests that corals might also be able to control ammonium fluxes to the symbionts by varying the expression level of an ammonium transporter at the symbiosome membrane (Thies et al, 2022).…”

Endosymbiont strategic shifts inhibit cooperation during coral bleaching recovery

“…6). At ambient conditions, corals invest ATP in regulating inorganic nitrogen and carbon inside the symbiosome [77, 78], while the symbiont translocates much of its resulting photosynthate back to the coral [13] (Fig. 6A).…”

Characterization of 3 different types of aquaporins in Carcinus maenas and their potential role in osmoregulation

“…Chloride ions crossing the apical membrane through Na + /K + /2Clcotransporter activity are moved into the hemolymph across basolateral Clchannels due to the electronegativity of the cytosol relative to the hemolymph (Lucu and Siebers, 1987;Onken et al, 1991;Riestenpatt et al, 1996). Apical Na + /H + and Cl -/HCO3exchangers also contribute to the absorption of Na + /Clfrom the environment, linking carbonic anhydrase to the osmoregulatory process due to its ability to catalytically hydrate intracellular CO2 (either metabolically produced or sourced from the hemolymph through Rhesus-protein mediated diffusion into the cytosol; Endeward et al, 2008;Soupene et al, 2004;Thies et al, 2022) to form the counter-ions used by the exchangers (Henry, 2005(Henry, , 2001Henry et al, 2003;Lucu, 1989;Siebers et al, 1987). This mechanism (Fig.…”