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Transepithelial absorption of exogenous inorganic carbon in the ctenidium of the giant clam, Tridacna squamosa involves a basolateral electrogenic Na+–HCO3 cotransporter 1 that displays light-enhanced gene and protein expression levels

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Abstract

Giant clams live in symbiosis with phototrophic dinoflagellates. They need to increase the uptake of inorganic carbon (Ci) from the ambient seawater to support light-enhanced shell formation in the host and photosynthesis in the symbionts during illumination. The ctenidium is the major site of light-enhanced Ci absorption in the fluted giant clam, Tridacna squamosa. Catalyzed by dual-domain carbonic anhydrase, exogenous HCO3 is dehydrated to CO2, which permeates the apical membrane of the ctenidial epithelium and is rehydrated back to HCO3 in the cytoplasm. However, the molecular mechanism that transports cytoplasmic HCO3 through the basolateral membrane to the hemolymph has not been elucidated. We have obtained from the ctenidium of T. squamosa the complete cDNA coding sequence of a homolog of electrogenic Na+HCO3 cotransporter 1 (NBCe1-like), which comprised 3450 bp, encoding a protein (NBCe1-like) of 1142 amino acids and 128.9 kDa. NBCe1-like had a basolateral localization in epithelial cells covering the ctenidial filament and those surrounding the tertiary water channels. Light exposure led to significant increases in the transcript and protein levels of NBCe1-like/NBCe1-like in the ctenidium of T. squamosa, indicating that NBCe1-like could be involved in the increased transport of cytoplasmic HCO3 across the basolateral membrane into the hemolymph during illumination. Additionally, NBCe1-like might also participate in light-enhanced NO3 absorption in T. squamosa, due to the replacement of aspartate (residue 585) with glutamine. Exogenous NO3 could be absorbed by the ctenidial epithelial cells through the apical H+:NO3 cotransporter (SIALIN) and then transported through the basolateral NBCe1-like to the hemolymph.

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References

  • Alper SL, Sharma AK (2013) The SLC26 gene family of anion transporters and channels. Mol Aspects Med 34:494–515

    CAS  PubMed  PubMed Central  Google Scholar 

  • Barott KL, Perez SO, Linsmayer LB, Tresguerres M (2015) Differential localization of ion transporters suggests distinct cellular mechanisms for calcification and photosynthesis between two coral species. Am J Physiol Regul Integr Comp Physiol 309:235–246

    Google Scholar 

  • Boo MV, Hiong KC, Goh EJK, Choo CYL, Wong WP, Chew SF, Ip YK (2018) The ctenidium of the giant clam, Tridacna squamosa, expresses an ammonium transporter 1 that displays light-suppressed gene and protein expression and may be involved in ammonia excretion. J Comp Physiol B 188:765–777

    CAS  PubMed  Google Scholar 

  • Boo MV, Hiong KC, Wong WP, Chew SF, Ip YK (2019) Shell formation in the giant clam, Tridacna squamosa, may involve an apical Na+/Ca2+ exchanger 3 homolog in the shell-facing epithelium of the whitish inner mantle, which displays light-enhanced gene and protein expression. Coral Reefs 38:1173–1186

    Google Scholar 

  • Boron WF, Chen L, Parker MD (2009) Modular structure of sodium-coupled bicarbonate transporters. J Exp Biol 212:1697–1706. https://doi.org/10.1242/jeb.028563

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brahmi C, Chapron L, Le Moullac G, Soyez C, Beliaeff B, Lazareth CE, et al (2019) Effects of temperature and pCO2 on the respiration, biomineralization and photophysiology of the giant clam Tridacna maxima. bioRxiv 672907

  • Brauner CJ, Shartau RB, Damsgaard C, Esbaugh AJ, Wilson RW, Grosell M (2019) Acid-base physiology and CO2 homeostasis: regulation and compensation in response to elevated environmental CO2. In: Grosell M, Munday PL, Farrell AP, Brauner CJ (eds) Fish physiology, vol 37. Academic Press, Cambridge, pp 69–132

    Google Scholar 

  • Chan CYL, Hiong KC, Boo MV, Choo CYL, Wong WP, Chew SF, Ip YK (2018) Light exposure enhances urea absorption in the fluted giant clam, Tridacna squamosa, and up-regulates the protein abundance of a light-dependent urea active transporter, DUR3-like, in its ctenidium. J Exp Biol 221:jeb176313. https://doi.org/10.1242/jeb.176313

    Article  PubMed  Google Scholar 

  • Chan CYL, Hiong KC, Choo CYL, Boo MV, Wong WP, Chew SF, Ip YK (2019) Increased apical sodium-dependent glucose transporter abundance in the ctenidium of the giant clam Tridacna squamosa upon illumination. J Exp Biol 222:jeb195644. https://doi.org/10.1242/jeb.195644

    Article  PubMed  Google Scholar 

  • Chan CYL, Hiong KC, Choo CYL, Boo MV, Wong WP, Chew SF, Ip YK (2020a) Light-enhanced phosphate absorption in the fluted giant clam, Tridacna squamosa, entails an increase in the expression of sodium-dependent phosphate transporter 2a in its colourful outer mantle. Coral Reefs. https://doi.org/10.1007/s00338-020-01930-w

    Article  Google Scholar 

  • Chan JW, Boo MV, Wong WP, Chew SF, Ip YK (2020) Illumination enhances the protein abundance of sarcoplasmic reticulum Ca2+-ATPases-like transporter in the ctenidium and whitish inner mantle of the giant clam, Tridacna squamosa, to augment exogenous Ca2+ uptake and shell formation, respectively. Comp Biochem Physiol Part A Mol Integ Physiol 251:110811

    Google Scholar 

  • Chang MH, DiPiero J, Sonnichsen FD, Romero MF (2008) Entry to “HCO3 tunnel” revealed by SLC4A4 human mutation and structural model. J Biol Chem 283:18402–18410. https://doi.org/10.1074/jbc.M709819200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chernova MN, Jiang L, Friedman DJ, Darman RB, Lohi H, Kere J, Vandorpe DH, Alper SL (2005) Functional comparison of mouse slc26a6 anion exchanger with human SLC26A6 polypeptide variants: differences in anion selectivity, regulation, and electrogenicity. J Biol Chem 280:8564–8580

    CAS  PubMed  Google Scholar 

  • Choi I, Aalkjær C, Boulpaep EL, Boron WF (2000) An electroneutral sodium/bicarbonate cotransporter NBCn1 and associated sodium channel. Nature 405:571–575

    CAS  PubMed  Google Scholar 

  • Choi I, Kobayashi C, Jacovich M, Boron WF (2001) Structure/function analysis of an electroneutral Na/HCO3 cotransporter (NBCn1) (Abstract). FASEB J 15:446

    Google Scholar 

  • Choi I, Yang HS, Boron WF (2006) The electrogenicity of the sodium/bicarbonate cotransporter NBCe1 is confined in the conserved transmembrane domains. FASEB J 20:1232

    Google Scholar 

  • Cudennec B, Rousseau M, Lopez E, Fouchereau-Peron M (2006) CGRP stimulates gill carbonic anhydrase activity in molluscs via a common CT/CGRP receptor. Peptides 27:2678–2682

    CAS  PubMed  Google Scholar 

  • de Goeij JM, van Oevelen D, Vermeij MJ, Osinga R, Middelburg JJ, de Goeij AF, Admiraal W (2013) Surviving in a marine desert: the sponge loop retains resources within coral reefs. Science 342:108–110

    PubMed  Google Scholar 

  • Deane EM, O’Brien RW (1980) Composition of the hemolymph of Tridacna maxima (Mollusca: Bivalvia). Comp Biochem Physiol 66:339–341. https://doi.org/10.1016/0300-9629(80)90173-5

    Article  Google Scholar 

  • DeBoer TS, Baker AC, Erdmann MV, Jones PR, Barber PH (2012) Patterns of Symbiodinium distribution in three giant clam species across the biodiverse Bird’s Head region of Indonesia. Mar Ecol Prog Ser 444:117–132

    CAS  Google Scholar 

  • Fitt WK, Rees TAV, Yellowless D (1995) Relationship between pH and the availability of dissolved inorganic nitrogen in the zooxanthella-giant clam symbiosis. Limnol Oceanogr 40:976–982. https://doi.org/10.4319/lo.1995.40.5.0976

    Article  CAS  Google Scholar 

  • Furla P, Galgani I, Durand I, Allemand D (2000a) Sources and mechanisms of inorganic carbon transport for coral calcification and photosynthesis. J Exp Biol 203:3445–3457

    CAS  PubMed  Google Scholar 

  • Furla P, Allemand D, Orsenigo MN (2000b) Involvement of H+-ATPase and carbonic anhydrase in inorganic carbon uptake for endosymbiont photosynthesis. Am J Physiol Regul Integr Comp Physiol 278:870–881

    Google Scholar 

  • Griffiths CL, Klumpp DW (1996) Relationships between size, mantle area and zooxanthellae numbers in five species of giant clam (Tridacnidae). Mar Eco Prog Ser 137:139–147

    Google Scholar 

  • Gross E, Hawkins K, Pushkin A, Sassani P, Dukkipati R, Abuladze N, Hopfer U, Kurtz I (2001a) Phosphorylation of Ser982 in the sodium bicarbonate cotransporter kNBC1 shifts the HCO3: Na+ stoichiometry from 3: 1 to 2: 1 in murine proximal tubule cells. J Physiol 537:659–665

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gross E, Hawkins K, Abuladze N, Pushkin A, Cotton CU, Hopfer U, Kurtz I (2001b) The stoichiometry of the electrogenic sodium bicarbonate cotransporter NBC1 is cell-type dependent. J Physiol 531:597–603

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guibert I, Lecellier G, Torda G, Pochon X, Berteaux-Lecellier V (2020) Metabarcoding reveals distinct microbiotypes in the giant clam Tridacna maxima. Microbiome 8:1–14

    Google Scholar 

  • Hernawan UE (2008) Review: symbiosis between the giant clams (Bivalvia: Cardiidae) and zooxanthallae (Dinophyceae). Biodiversitas 9:53–58

    Google Scholar 

  • Hiong KC, Choo CYL, Boo MV, Ching B, Wong WP, Chew SF, Ip YK (2017a) A light-dependent ammonia-assimilating mechanism in the ctenidia of a giant clam. Coral Reefs 36:311–323

    Google Scholar 

  • Hiong KC, Cao-Pham AH, Choo CYL, Boo MV, Wong WP, Chew SF, Ip YK (2017b) Light-dependent expression of a Na+/H+ exchanger 3-like transporter in the ctenidium of the giant clam, Tridacna squamosa, can be related to increased H+ excretion during light-enhanced calcification. Phys Rep 5:e13209. https://doi.org/10.14814/phy2.13209

    Article  CAS  Google Scholar 

  • Hirata T, Kaneko T, Ono T, Nakazato T, Furukawa N, Hasegawa S, Wakabayashi S, Shigekawa M, Chang M, Romero MF, Hirose S (2003) Mechanism of acid adaptation of a fish living in a pH 3.5 lake. Am J Physiol Regul Integr Comp Physiol 284:1199–1212

    Google Scholar 

  • Holt AL, Vahidinia S, Gagnon YL, Morse DE, Sweeney AM (2014) Photosymbiotic giant clams are transformers of solar flux. J R Soc Interface 11:20140678

    PubMed  PubMed Central  Google Scholar 

  • Ikeda S, Yamashita H, Kondo SN, Inoue K, Morishima SY, Koike K (2017) Zooxanthellal genetic varieties in giant clams are partially determined by species-intrinsic and growth-related characteristics. PLOS ONE 12:e0172285

    PubMed  PubMed Central  Google Scholar 

  • Ip YK, Hiong KC, Goh EJK, Boo MV, Choo CYL, Ching B, Wong WP, Chew SF (2017) The whitish inner mantle of the giant clam Tridacna squamosa expresses an apical Plasma Membrane Ca2+-ATPase (PMCA) which displays light-dependent gene and protein expressions. Front Physiol 8:781. https://doi.org/10.3389/fphys.2017.00781

    Article  PubMed  PubMed Central  Google Scholar 

  • Ip YK, Hiong KC, Lim LJY, Choo CYL, Boo MV, Wong WP, Neo ML, Chew SF (2018) 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. Gene 659:137–148. https://doi.org/10.1016/j.gene.2018.03.054

    Article  CAS  PubMed  Google Scholar 

  • Ip YK, Hiong KC, Teng JHQ, Boo MV, Choo CYL, Wong WP, Chew SF (2020) The fluted giant clam (Tridacna squamosa) increases nitrate absorption and upregulates the expression of a homolog of SIALIN (H+:2NO3 cotransporter) in the ctenidium during light exposure. Coral Reefs 39:451–465. https://doi.org/10.1007/s00338-020-01907-9

    Article  Google Scholar 

  • Jantzen C, Wild C, Mohammed E, Roa-Quiaoit HA, Haacke C, Richter C (2008) Photosynthetic performance of giant clams, Tridacna maxima and T. squamosa. Red Sea Mar Biol 155:211–221

    Google Scholar 

  • Klumpp DW, Griffiths CL (1994) Contributions of phototrophic and heterotrophic nutrition to the metabolic and growth requirements of four species of giant clam (Tridacnidae). Mar Ecol Prog Ser 115:103–115

    Google Scholar 

  • Koh CZY, Hiong KC, Choo CYL, Boo MV, Wong WP, Chew SF, Neo ML, Ip YK (2018) Molecular characterization of a Dual Domain Carbonic Anhydrase from the ctenidium of the giant clam, Tridacna squamosa, and its expression levels after light exposure, cellular localization, and possible role in the uptake of exogenous inorganic carbon. Front Physiol 9:281. https://doi.org/10.3389/fphys.2018.00281

    Article  PubMed  PubMed Central  Google Scholar 

  • Kurtz I, Zhu Q (2013) Structure, function, and regulation of the SLC4 NBCe1 transporter and its role in causing proximal renal tubular acidosis. Curr Opin Nephrol Hypertens 22:572

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lee SK, Boron WF, Parker MD (2013) Substrate specificity of the electrogenic sodium/bicarbonate cotransporter NBCe1-A (SLC4A4, variant A) from humans and rabbits. Am J Physiol Renal Physiol 304:883–899

    Google Scholar 

  • Leggat W, Badger MR, Yellowlees D (1999) Evidence for an inorganic carbon-concentrating mechanism in the symbiotic dinoflagellate Symbiodinium sp. Plant Physiol 121:1247–1255. https://doi.org/10.1104/pp.121.4.1247

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li HC, Worrell RT, Matthews JB, Husseinzadeh H, Neumeier L, Petrovic S, Conforti L, Soleimani M (2004) Identification of a carboxyl-terminal motif essential for the targeting of Na+-cotransporter NBC1 to the basolateral membrane. J Biol Chem 279:43190–43197

    CAS  PubMed  Google Scholar 

  • Li HC, Collier JH, Shawki A, Rudra JS, Li EY, Mackenzie B, Soleimani M (2009) Sequence- or position-specific mutations in the carboxyl-terminal FL motif of the kidney sodium bicarbonate cotransporter (NBC1) disrupt its basolateral targeting and alpha-helical structure. J Membr Biol 228:111–124. https://doi.org/10.1007/s00232-009-9164-6

    Article  CAS  PubMed  Google Scholar 

  • Lim SSQ, Huang D, Soong K, Neo ML (2019) Diversity of endosymbiotic symbiodiniaceae in giant clams at Dongsha Atoll, northern South China Sea. Symbiosis 78:251–262

    Google Scholar 

  • Lu J, Boron WF (2007) The reversible and irreversible interactions of DIDS with the human electrogenic Na/HCO3 cotransporter (hNBCe1-A): importance of K558, K559 and K562 within the KKMIK motif of transmembrane segment 5. Am J Physiol Cell Physiol 292:1787–1798

    Google Scholar 

  • Maetz J (1971) Fish gills: mechanisms of salt transfer in fresh water and sea water. Philos Trans R Soc Lond B Biol Sci 262:209–249

    CAS  Google Scholar 

  • Morishima SY, Yamashita H, O-hara S, Nakamura Y, Quek VZ, Yamauchi M, Koike K (2019) Study on expelled but viable zooxanthellae from giant clams, with an emphasis on their potential as subsequent symbiont sources. PLOS ONE 14:e0220141

    CAS  PubMed  PubMed Central  Google Scholar 

  • Müller-Berger S, Coppola S, Samarzija I, Seki G, Frömter E (1997) Partial recovery of in vivo function by improved incubation conditions of isolated renal proximal tubule. I. Change of amiloride-inhibitable K+ conductance. Pflügers Arch 434:373–382

    PubMed  Google Scholar 

  • Muller-Berger S, Nesterov VV, Frömter E (1997) Partial recovery of in vivo function by improved incubation conditions of isolated renal proximal tubule II change of Na-HCO3 cotransport stoichiometry and of response to acetazolamide. Pflügers Arch 434:383–391

    CAS  PubMed  Google Scholar 

  • Muller-Berger S, Ducoudret O, Diakov A, Frömter E (2001) The renal Na-HCO3cotransporter expressed in Xenopus laevis oocytes: change in stoichiometry in response to elevation of cytosolic Ca2+ concentration. Pflügers Arch 442:718–728

    CAS  PubMed  Google Scholar 

  • Neo ML, Eckman W, Vicentuan K, Teo SL-M, Todd PA (2015) The ecological significance of giant clams in coral reef ecosystems. Biol Conserv 181:111–123

    Google Scholar 

  • Norton JH, Shepherd MA, Long HM, Fitt WK (1992) The zooxanthellal tubular system in the giant clam. Biol Bull 183:503–506. https://doi.org/10.2307/1542028

    Article  CAS  PubMed  Google Scholar 

  • Ohana E, Yang D, Shcheynikov N, Muallem S (2009) Diverse transport modes by the solute carrier 26 family of anion transporters. J Physiol 587:2179–2185

    CAS  PubMed  Google Scholar 

  • Ohana E, Shcheynikov N, Yang D, So I, Muallem S (2011) Determinants of coupled transport and uncoupled current by the electrogenic SLC26 transporters. J Gen Physiol 137:239–251

    CAS  PubMed  PubMed Central  Google Scholar 

  • Perry SF, Shahsavarani A, Georgalis T, Bayaa M, Furimsky M, Thomas SLY (2003) Channels, pumps, and exchangers in the gill and kidney of freshwater fishes: their role in ionic and acid-base regulation. J Exp Zool A Comp Exp Biol 300:53–62

    CAS  PubMed  Google Scholar 

  • Piermarini PM, Choi I, Boron WF (2007) Cloning and characterization of an electrogenic Na/HCO3 cotransporter from the squid giant fiber lobe. Am J Physiol Cell Physiol 292:2032–2045

    Google Scholar 

  • Pochon X, Wecker P, Stat M, Berteaux-Lecellier V, Lecellier G (2019) Towards an in-depth characterization of Symbiodiniaceae in tropical giant clams via metabarcoding of pooled multi-gene amplicons. PeerJ 7:e6898. https://doi.org/10.7717/peerj.6898

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Poo JS, Choo CYL, Hiong KC, Boo MV, Wong WP, Chew SF, Ip YK (2020) Phototrophic potential and form II ribulose-1, 5-bisphosphate carboxylase/oxygenase expression in five organs of the fluted giant clam, Tridacna squamosa. Coral Reefs 39:361–374

    Google Scholar 

  • Poo JS, Boo MV, Chew SF, Ip YK (2021) Using form II ribulose-1,5-bisphosphate carboxylase /oxygenase to estimate the phototrophic potentials of Symbiodinium, Cladocopium and Durusdinium in various organs of the fluted giant clam, Tridacna squamosa, and to evaluate their responses to light upon isolation from the host. Coral reefs. https://doi.org/10.1007/s00338-020-02031-4

  • Rees TAV, Fitt WK, Baillie B, Yellowlees D (1993) A method for temporal measurement of haemolymph composition in the giant clam symbiosis and its application to glucose and glycerol levels during a diel cycle. Limnol Oceanogr 38:213–217

    CAS  Google Scholar 

  • Romero MF, Hediger MA, Boulpaep EL, Boron WF (1997) Expression cloning and characterization of a renal electrogenic Na+/HCO3 cotransporter. Nature 387:409–413

    CAS  PubMed  Google Scholar 

  • Romero MF, Chen AP, Parker MD, Boron WF (2013) The SLC4 family of bicarbonate (HCO3-) transporters. Mol Aspects Med 34:159–182

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rossbach S, Saderne V, Anton A, Duarte CM (2019) Light-dependent calcification in Red Sea giant clam Tridacna maxima. Biogeosciences 16:2635–2650. https://doi.org/10.5194/bg-16-2635-2019

    Article  CAS  Google Scholar 

  • Rossbach S, Subedi RC, Ng TK, Ooi BS, Duarte CM (2020) Iridocytes mediate photonic cooperation between giant clams (Tridacninae) and their photosynthetic symbionts. Front Mar Sci. https://doi.org/10.3389/fmars.2020.00465

    Article  Google Scholar 

  • Roughton FJW (1964) Transport of oxygen and carbon dioxide. Handbook of Physiology 1:767–825

    Google Scholar 

  • Sciortino CM, Romero MF (1999) Cation and voltage dependence of rat kidney electrogenic Na+-HCO3 cotransporter, rkNBC, expressed in oocytes. Am J Physiol Renal Physiol 277:611–623

    Google Scholar 

  • Skelton LA, Boron WF, Zhou Y (2010) Acid-base transport by the renal proximal tubule. J Nephrol 23(Suppl. 16):S4-18

    PubMed  PubMed Central  Google Scholar 

  • Tsirigos KD, Peters C, Shu N, Käll L, Elofsson A (2015) The TOPCONS web server for consensus prediction of membrane protein topology and signal peptides. Nucleic Acid Res 43:401–407

  • Umeki M, Yamashita H, Suzuki G, Sato T, Ohara S, Koike K (2020) Fecal pellets of giant clams as a route for transporting Symbiodiniaceae to corals. PloS One 15(12):e0243087. https://doi.org/10.1371/journal.pone.0243087

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Virkki LV, Choi I, Davis BA, Boron WF (2003) Cloning of a Na+-driven Cl/HCO3 exchanger from squid giant fiber lobe. Am J Physiol Cell Physiol 285:771–780

    Google Scholar 

  • Watson SA, Southgate PC, Miller GM, Moorhead JA, Knauer J (2012) Ocean acidification and warming reduce juvenile survival of the flutted giant clam Tridacna squamosa. Molluscan Res 32:177–180

    Google Scholar 

  • Watson SA (2015) Giant clams and rising CO2: light may ameliorate effects of ocean acidification on a solar-powered animal. PLOS ONE 10(6):e0128405. https://doi.org/10.1371/journal.pone.0128405

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weber M (2009) The biogeography and evolution of Symbiodinium in giant clams (Tridacnidae). Ph.D Thesis, UC Berkeley.

  • Yellowlees D, Dionisio-Sese ML, Masuda K, Maruyama T, Abe T, Baillie B, Tsuzuki M, Miyachi S (1993) Role of carbonic anhydrase in the supply of inorganic carbon to the giant clam—zooxanthellate symbiosis. Mar Biol 115:605–611

    CAS  Google Scholar 

  • Yang HS, Kim E, Lee S, Park HJ, Cooper DS, Rajbhandari I, Choi I (2009) Mutation of Aspartate 555 of the Sodium/Bicarbonate Transporter SLC4A4/NBCe1 Induces Chloride Transport. J Biol Chem 284:15970–15979

  • Zhu Q, Azimov R, Kao L, Newman D, Liu W, Abuladze N, Pushkin A, Kurtz I (2009) NBCe1-A transmembrane segment 1 lines the ion translocation pathway. J Biol Chem 284:8918–8929. https://doi.org/10.1074/jbc.M806674200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu Q, Kao L, Azimov R, Abuladze N, Newman D, Pushkin A, Liu W, Chang C, Kurtz I (2010) Structural and functional characterization of the C-terminal transmembrane region of NBCe1-A. J Biol Chem 285:37178–37187. https://doi.org/10.1074/jbc.M110.169201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu Q, Liu W, Kao L, Azimov R, Newman D, Abuladze N, Kurtz I (2013) Topology of NBCe1 protein transmembrane segment 1 and structural effect of proximal renal tubular acidosis (pRTA) S427L mutation. J Biol Chem 288:7894–7906. https://doi.org/10.1074/jbc.M112.404533

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zoccola D, Ganot P, Bertucci A, Caminiti-Segonds N, Techer N, Voolstra CR, Aranda M, Tambutté E, Allemand D, Casey JR, Tambutté S (2015) Bicarbonate transporters in corals point towards a key step in the evolution of cnidarian calcification. Sci Rep 5:9983

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This study was supported by the Singapore Ministry of Education through grants to Y. K. Ip (R-154-000-A37-114 and R-154-000-B69-114) and to S. F. Chew (NIE AcRF RI3/19CSF).

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Boo, M.V., Chew, S.F. & Ip, Y.K. Transepithelial absorption of exogenous inorganic carbon in the ctenidium of the giant clam, Tridacna squamosa involves a basolateral electrogenic Na+–HCO3 cotransporter 1 that displays light-enhanced gene and protein expression levels. Coral Reefs 40, 1849–1865 (2021). https://doi.org/10.1007/s00338-021-02142-6

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