Molecular characterization, light-dependent expression, and cellular localization of a host vacuolar-type H + -ATPase (VHA) subunit A in the giant clam, Tridacna squamosa , indicate the involvement of the host VHA in the uptake of inorganic carbon and its supply to the symbiotic zooxanthellae

Ip, Yuen K.; Hiong, Kum C.; Lim, Leon J.Y.; Choo, Celine Yen Ling; Boo, Mel V.; Wong, Wai P.; Neo, Mei Lin; Chew, Shit F.

doi:10.1016/j.gene.2018.03.054

Cited by 35 publications

(48 citation statements)

References 56 publications

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“…6. As recently proposed (Ip et al, 2017(Ip et al, , 2018, CA-2-like proteins present in epithelial Z-tubule cells likely catalyze the hydration of CO 2 produced in host clam cells into H + and HCO 3 − . H + is then actively transported by VHA into the Z-tubule lumen, resulting in tubular acidification as well as the generation of an electromotive force for HCO 3 − secretion.…”

Section: Discussionmentioning

confidence: 72%

“…Immunolabeling in siphonal mantle showed VHA is highly expressed in the apical membrane of epithelial Z-tubule cells which contain Symbiodinium (Fig. 4), similar to VHA B in T. squamosa (Ip et al, 2018).…”

Section: Vha Is Highly Abundant In T Maxima Siphonal Mantle Tubulesmentioning

confidence: 66%

“…Within the tubule lumen, host-derived extracellular CAs could then dehydrate HCO 3 − and H + back to CO 2 , which then diffuses into Symbiodinium to be fixed into organic carbon compounds during photosynthesis. Additionally, HCO 3 − present in the Z-tubule lumen derived from external seawater might also be dehydrated into CO 2 and taken up by Symbiodinium (Ip et al, 2018).…”

Section: Discussionmentioning

confidence: 99%

“…Tridacnid clams have also been hypothesized to utilize CCMs to promote Symbiodinium photosynthesis (Leggat et al, 1999;Yellowlees et al, 1993). The evidence includes the high abundance of carbonic anhydrases (CAs) in the siphonal mantle (Yellowlees et al, 1993), as well as a recent paper reporting the presence of VHA subunit A (VHA A ) in epithelial cells of Symbiodinium-containing Z-tubules (Ip et al, 2018). Furthermore, freshly isolated Symbiodinium sustain much greater photosynthetic rates in the presence of CO 2 versus HCO 3 − (Leggat et al, 1999;Yellowlees et al, 1993), which is consistent with a CCM controlled by the clam.…”

Section: Introductionmentioning

confidence: 99%

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

Armstrong

Roa

Stillman

et al. 2018

Journal of Experimental Biology

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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.

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Section: Discussionmentioning

confidence: 72%

Section: Vha Is Highly Abundant In T Maxima Siphonal Mantle Tubulesmentioning

confidence: 66%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

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

Armstrong

Roa

Stillman

et al. 2018

Journal of Experimental Biology

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“…Slides were mounted in ProLong Gold Antifade Mountant (Life Technologies, USA) and cured in the dark at room temperature prior to storing at 4°C for further image acquisition. Image acquisition was conducted with a fluorescence microscope (Olympus BX60 equipped with a DP73 CCD digital camera) with the appropriate fluorescent filter sets (Ip et al, 2018). A DIC slider (U-DICT, Olympus) was used to produce differential interference contrast (DIC) images of the tissue structures such as ctenidial filaments and water channels.…”

Section: Immunofluorescence Microscopymentioning

confidence: 99%

With illumination, the fluted giant clam,Tridacna squamosa, upregulates the protein abundance of an apical Na+: glucose cotransporter 1 homolog in its ctenidium, and increases exogenous glucose absorption that can be impeded by urea

Chan

Hiong

Choo

et al. 2019

Journal of Experimental Biology

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Giant clams contain phototrophic zooxanthellae, and live in nutrientdeficient tropical waters where light is available. We obtained the complete cDNA coding sequence of a homolog of mammalian sodium/ glucose cotransporter 1 (SGLT1)-SGLT1-likefrom the ctenidium of the fluted giant clam, Tridacna squamosa. SGLT1-like had a host origin and was expressed predominantly in the ctenidium. Molecular characterizations reveal that SGLT1-like of T. squamosa could transport urea, in addition to glucose, as other SGLT1s do. It has an apical localization in the epithelium of ctenidial filaments and water channels, and the apical anti-SGLT1-like immunofluorescence was stronger in individuals exposed to light than to darkness. Furthermore, the protein abundance of SGLT1-like increased significantly in the ctenidium of individuals exposed to light for 12 h, although the SGLT1like transcript level remained unchanged. As expected, T. squamosa could perform light-enhanced glucose absorption, which was impeded by exogenous urea. These results denote the close relationships between light-enhanced glucose absorption and light-enhanced SGLT1-like expression in the ctenidium of T. squamosa. Although glucose absorption could be trivial compared with the donation of photosynthates from zooxanthellae in symbiotic adults, SGLT1-like might be essential for the survival of aposymbiotic larvae, leading to its retention in the symbiotic stage. A priori, glucose uptake through SGLT1-like might be augmented by the surface microbiome through nutrient cycling, and the absorbed glucose could partially fulfill the metabolic needs of the ctenidial cells. Additionally, SGLT1-like could partake in urea absorption, as T. squamosa is known to conduct lightenhanced urea uptake to benefit the nitrogen-deficient zooxanthellae.

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Effects of the daily light-dark cycle on rhythms of behavior and physiology in boring giant clam Tridacna crocea

Li,

Yang,

Hong

et al. 2024

Mar Biol

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Molecular characterization, light-dependent expression, and cellular localization of a host vacuolar-type H + -ATPase (VHA) subunit A in the giant clam, Tridacna squamosa , indicate the involvement of the host VHA in the uptake of inorganic carbon and its supply to the symbiotic zooxanthellae

Cited by 35 publications

References 56 publications

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

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

With illumination, the fluted giant clam,Tridacna squamosa, upregulates the protein abundance of an apical Na+: glucose cotransporter 1 homolog in its ctenidium, and increases exogenous glucose absorption that can be impeded by urea

Effects of the daily light-dark cycle on rhythms of behavior and physiology in boring giant clam Tridacna crocea

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