Symbiont photosynthesis in giant clams is promoted by V-type H+-ATPase from host cells

Abstract

Giant clams (genus ) are the largest living bivalves and, like reef-building corals, host symbiotic dinoflagellate algae () that significantly contribute to their energy budget. In turn, rely on the host to supply inorganic carbon (C) for photosynthesis. In corals, host 'proton pump' vacuolar-type H-ATPase (VHA) is part of a carbon-concentrating mechanism (CCM) that promotes photosynthesis. Here, we report that VHA in the small giant clam () similarly promotes photosynthesis. VHA was abundantly expressed in the apical membrane of epithelial cells of's siphonal mantle tubule system, which harbors Furthermore, application of the highly specific pharmacological VHA inhibitors bafilomycin A1 and concanamycin A significantly reduced photosynthetic O production by ∼40%. Together with our observation that exposure to light increased holobiont aerobic metabolism ∼5-fold, and earlier estimates that translocated fixed carbon exceeds metabolic demand, we conclude that VHA activity in the siphonal mantle confers strong energetic benefits to the host clam through increased supply of C to algal symbionts and subsequent photosynthetic activity. The convergent role of VHA in promoting photosynthesis in the giant clam siphonal mantle tubule system and coral symbiosome suggests that VHA-driven CCM is a common exaptation in marine photosymbioses that deserves further investigation in other taxa.

Shedding light: a phylotranscriptomic perspective illuminates the origin of photosymbiosis in marine bivalves

“…Molecular level parallel evolution has been shown in photosymbiotic systems. For example, both corals and giant clams repurpose the expression of the vacuolar H + -ATPase gene (VHA) to facilitate their carbon concentrating process and promote algal photosynthesis, even though the two lineages are very distantly related [39,40]. Our analyses further support that VHA is a conserved gene, ancestral to bivalves, corals, and other animals.…”

“…We also assessed the evolution of one particular gene that is known to promote photosymbiosis in Tridacna [39] and corals [40], the V-type H + -ATPase (VHA). We identified VHA genes from our Tridacninae and Fraginae species by running a BLAST search using the scleractinian coral (Acropora yongei) VHA amino acid sequence reported in [40].…”

Shedding light: A phylotranscriptomic perspective illuminates the origin of photosymbiosis in marine bivalves

“…Molecular level parallel evolution has been shown in photosymbiotic systems. For example, both corals and giant clams repurpose the expression of the vacuolar H+-ATPase gene (VHA) to facilitate their carbon concentrating process and promote algal photosynthesis, even though the two lineages are very distantly related [59,60]. Our analyses further support that VHA is a conserved gene, ancestral to bivalves, corals, and other animals.…”

“…We also assessed the evolution of one particular gene that is known to promote photosymbiosis in Tridacna [59] and corals [60], the V-type H+-ATPase (VHA). We identified VHA genes from our Tridacninae and Fraginae species by running a BLAST search using the scleractinian coral (Acropora yongei) VHA amino acid sequence reported in [60].…”

Shedding light: A phylotranscriptomic perspective illuminates the origin of photosymbiosis in marine bivalves

“…Molecular level parallel evolution has been shown in photosymbiotic systems. For example, both corals and giant clams repurpose the expression of the vacuolar H+-ATPase gene (VHA) to facilitate their carbon concentrating process and promote algal photosynthesis, even though the two lineages are very distantly related [67][68]. In contrast with the relatively labile shell and mantle adaptations, it is possible that the evolution of host metabolomic and developmental adaptations are more constrained genetically, resulting in similar mechanisms in diverse animal groups.…”