Coral host cells acidify symbiotic algal microenvironment to promote photosynthesis

Abstract

Symbiotic dinoflagellate algae residing inside coral tissues supply the host with the majority of their energy requirements through the translocation of photosynthetically fixed carbon. The algae, in turn, rely on the host for the supply of inorganic carbon. Carbon must be concentrated as CO 2 in order for photosynthesis to proceed, and here we show that the coral host plays an active role in this process. The host-derived symbiosome membrane surrounding the algae abundantly expresses vacuolar H + -ATPase (VHA), which acidifies the symbiosome space down to pH ∼4. Inhibition of VHA results in a significant decrease in average H + activity in the symbiosome of up to 75% and a significant reduction in O 2 production rate, a measure of photosynthetic activity. These results suggest that host VHA is part of a previously unidentified carbon concentrating mechanism for algal photosynthesis and provide mechanistic evidence that coral host cells can actively modulate the physiology of their symbionts.

Novel and potential physiological roles of vacuolar-type H+-ATPase in marine organisms

“…4) involves acidification of the symbiosome space by VHA to pH∼4, which presumably energizes the parallel transport of HCO 3 − and favours the chemical speciation of DIC into CO 2 . The evidence in support of this mechanism includes a high abundance of VHA in symbiosome membranes of gastrodermal cells, alkalinization of the symbiosome space from pH∼4 to pH∼5 in response to bafilomycin (a specific inhibitor of VHA) in isolated cell experiments, and a significant decline in O 2 production in coral branches exposed to bafilomycin (Barott et al, 2015). This mechanism has been reported for two coral species belonging to the two different coral clades, robust and complex (Barott et al, 2015), so it is likely to apply to most, if not all, reef-building corals.…”

“…The evidence in support of this mechanism includes a high abundance of VHA in symbiosome membranes of gastrodermal cells, alkalinization of the symbiosome space from pH∼4 to pH∼5 in response to bafilomycin (a specific inhibitor of VHA) in isolated cell experiments, and a significant decline in O 2 production in coral branches exposed to bafilomycin (Barott et al, 2015). This mechanism has been reported for two coral species belonging to the two different coral clades, robust and complex (Barott et al, 2015), so it is likely to apply to most, if not all, reef-building corals. Furthermore, given that most marine photosynthesizing organisms require a CCM (Reinfelder, 2011), and that VHA is evolutionarily conserved in eukaryotic cells, the mechanism described for carbon concentrating in corals may be widespread.…”

“…However, this presents a physiological challenge, as there are no known molecular mechanisms to actively transport gases such as CO 2 and, at the pH of seawater and coral cell cytoplasm, the most abundant dissolved inorganic carbon (DIC) species is, by far, HCO 3 − . Recently, VHA in the host-derived symbiosome membrane has been shown to promote Symbiodinium photosynthesis (Barott et al, 2015). The proposed mechanism (Fig.…”

Ammonia excretion in mytilid mussels is facilitated by ciliary beating

“…For detection of the VHA B-subunit, custom-made purified polyclonal rabbit antibodies against the peptide AREEVPGRRGFPGY were used ( protein size 55 kDA). These antibodies specifically recognize VHA B in a variety of diverse organisms including coral, bone-eating worms and sharks (Tresguerres et al, 2013;Roa et al, 2014;Barott et al, 2015). Additionally, commercially available polyclonal rabbit antibodies against mammalian α-subunit of sodium/potassium ATPase (NKA; α300, Santa Cruz Biotechnology, Dallas, TX, USA) and human carbonic anhydrase II (CA II; Rockland, Gilbertsville, PA, USA) were used recognizing proteins of the expected sizes of approximately 116 and 36 kDa, respectively.…”

Quantification of dimethyl sulfide (DMS) production in the sea anemone <i>Aiptasia</i> sp. to simulate the sea-to-air flux from coral reefs

“…1). It has been demonstrated that the coral host not only controls the population size of various Symbiodinium clades inside the symbiosomes (Kemp et al, 2014), but it also actively modifies the microenvironment on their surface (Barott et al, 2015), both with consequences for DMSP concentration and DMS production. Furthermore, DMS production is significantly different between the Symbiodinium clades (Table 2) so that the relative abundance of clade A1 affected coral-driven sea-to-air DMS fluxes (see N A1 in Fig.…”