Skip to main content
SpringerLink
Log in

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

  • Original Paper
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

Ammonium transporters (AMTs) can participate in ammonia uptake or excretion across the plasma membrane of prokaryotic, plant and invertebrate cells. The giant clam, Tridacna squamosa, harbors nitrogen-deficient symbiotic zooxanthellae, and normally conducts light-enhanced ammonia absorption to benefit the symbionts. Nonetheless, it can excrete ammonia when there is a supply of exogenous nitrogen or exposed to continuous darkness. This study aimed to elucidate the role of AMT1 in the ctenidium of T. squamosa by cloning and characterizing the AMT1/AMT1, determining its subcellular localization, and examining changes in its transcript and protein expression levels in response to light exposure. The cDNA coding sequence of AMT1 from T. squamosa consisted of 1527 bp and encoded 508 amino acids of 54.6 kDa. AMT1-immunofluorescence was detected mainly at the apical epithelium of ctenidial filaments, and it decreased significantly after 12 h of exposure to light. By contrast, the epithelial cells surrounding the tertiary water channels in the ctentidium, which are known to exhibit light-enhanced glutamine synthetase expression and take part in the assimilation of exogenous ammonia in light, did not display any AMT1-immunolabelling. Furthermore, the transcript level and protein abundance of ctenidial AMT1/AMT1 decreased significantly at the 6th and 12th h of light exposure. Taken together, these results indicate that AMT1 might participate in ammonia excretion instead of ammonia absorption and assimilation in T. squamosa. It is probable that the expression levels of AMT1/AMT1 need to be down-regulated during light exposure to achieve light-enhanced ammonia uptake.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Akgun U, Khademi S (2011) Periplasmic vestibule plays an important role for solute recruitment, selectivity, and gating in the Rh/Amt/MEP superfamily. Proc Natl Acad Sci USA 108:3970–3975

    Article  PubMed  Google Scholar 

  • Andrade SLA, Einsle O (2009) The Amt/Mep/Rh family of ammonium transport proteins (Review). Mol Membr Biol 24:357–365

    Article  CAS  Google Scholar 

  • Andrade SLA, Dickmanns A, Ficner R, Einsle O (2005) Crystal structure of the archaeal ammonium transporter Amt-1 from Archaeoglobus fulgidus. Proc Natl Acad Sci USA 102:14994–14999

    Article  PubMed  CAS  Google Scholar 

  • Baday S, Wang S, Lamoureux G, Bernèche S (2013) Different hydration patterns in the pores of AmtB and RhCG could determine their transport mechanisms. Biochemistry 52:7091–7098

    Article  PubMed  CAS  Google Scholar 

  • Belda CA, Lucas JS, Yellowlees D (1993) Nutrient limitation in the giant clam–zooxanthellae symbiosis: effects of nutrient supplements on growth of the symbiotic partners. Mar Biol 117:655–664

    Article  Google Scholar 

  • Bishop SH, Ellis LL, Burcham JM (1983) Amino acid metabolism in molluscs. In: Hochachka PW (ed) The mollusca, 1st edn. Elsevier, New York, pp 243–327

    Google Scholar 

  • Blakey D, Leech A, Thomas GA, Coutts G, Findlay K, Merrick M (2002) Purification of the Escherichia coli ammonium transporter AmtB reveals a trimeric stoichiometry. Biochem J 364:527–535

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Boo MV, Hiong KC, Choo CYL, Cao-Pham AH, Wong WP, Chew SF (2017) The inner mantle of the giant clam, Tridacna squamosa, expresses a basolateral Na+/K+-ATPase α-subunit, which displays light-dependent gene and protein expression along the shell-facing epithelium. PloS One. https://doi.org/10.1371/journal.pone.0186865

    Article  PubMed  PubMed Central  Google Scholar 

  • Bu Y, Sun B, Zhou A, Zhang X, Lee I, Liu S (2013) Identification and characterization of a PutAMT1;1 gene from Puccinellia tenuiflora. PloS One. https://doi.org/10.1371/journal.pone.0083111

    Article  PubMed  PubMed Central  Google Scholar 

  • Campbell JW (1991) Excretory nitrogen metabolism. In: Prosser CL (ed) Comparative animal physiology, 4th edn. Wiley, New York, pp 277–324

    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, and up-regulates the protein abundance of a light-dependent urea active transporter, DUR3-like, in its ctenidium. J Exp Biol 221(8):jeb176313

    Article  PubMed  Google Scholar 

  • Chasiotis H, Ionescu A, Misyura L, Bui P, Fazio K, Wang J, Patrick M, Weihrauch D, Donini A (2016) An animal homolog of plant Mep/Amt transporters promotes ammonia excretion by the anal papillae of the disease vector mosquito Aedes aegypti. J Exp Biol 219:1346–1355

    Article  PubMed  Google Scholar 

  • Chew SF, Ip YK (2014) Excretory nitrogen metabolism and defence against ammonia toxicity in air-breathing fishes. J Fish Biol 84:603–638

    Article  PubMed  CAS  Google Scholar 

  • Davies PS (1991) Effect of daylight variations on the energy budgets of shallow-water corals. Mar Biol 108:137–144

    Article  Google Scholar 

  • Durant AC, Donini A (2018) Ammonia excretion in an osmoregulatory syncytium is facilitated by AeAmt2, a novel ammonia transporter in Aedes aegypti larvae. Front Physiol. https://doi.org/10.3389/fphys.2018.00339

    Article  PubMed  PubMed Central  Google Scholar 

  • Evans DH, Piermarini PM, Choe KP (2005) The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid–base regulation, and excretion of nitrogenous waste. Physiol Rev 85:97–177

    Article  PubMed  CAS  Google Scholar 

  • Falkowski PG (1997) Evolution of the nitrogen cycle and its influence on the biological sequestration of CO2 in the ocean. Nature 387:272–273

    Article  CAS  Google Scholar 

  • Fitt WK, Heslinga GA, Watson TC (1993a) Utilisation of dissolved inorganic nutrients in growth and mariculture of the tridacnid clam Tridacna derasa. Aquaculture 109:27–38

    Article  CAS  Google Scholar 

  • Fitt WK, Rees TAV, Braley RD, Lucas JS, Yellowlees D (1993b) Nitrogen flux in giant clams: size-dependency and relationship to zooxanthellae density and clam biomass in the uptake of dissolved inorganic nitrogen. Mar Biol 117:381–386

    CAS  Google Scholar 

  • Garvin JL, Burg MB, Knepper MA (1985) Ammonium replaces potassium in supporting sodium transport by the Na-K-ATPase of renal proximal straight tubules. Am J Physiol Renal Physiol 249:785–788

    Article  Google Scholar 

  • Gazzarrani S, Lejay L, Gojon A, Ninnemann O, Frommer WB, von Wirén N (1999) Three functional transporters for constitutive, diurnally regulated, and starvation-induced uptake of ammonium into Arabidopsis roots. Plant Cell 11:937–947

    Article  Google Scholar 

  • Hall JA, Kustu S (2011) The pivotal twin histidines and aromatic triad of the Escherichia coli ammonium channel AmtB can be replaced. Proc Natl Acad Sci USA 108:13270–13274

    Article  PubMed  Google Scholar 

  • Hall JA, Yan D (2013) The molecular basis of K+ exclusion by the Escherichia coli ammonium channel AmtB. J Biol Chem 288:14080–14086

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Han K, Croker BP, Clapp WL, Werner D, Sahni M, Kim J, Kim H, Handlogten ME, Weiner ID (2006) Expression of the ammonia transporter, Rh C glycoprotein, in normal and neoplastic human kidney. Clin J Am Soc Nephrol 17:2670–2679

    Article  CAS  Google Scholar 

  • Hastie LC, Heslinga GA, Watson TC (1988) Lab test result: fertilizer speeds clam growth. Micronesian Mariculture Demonstration Center Bulletin, vol 3, Micronesian Mariculture Demonstration Centre, Palau

    Google Scholar 

  • Hastie LC, Watson TC, Isamu T, Heslinga GA (1992) Effect of nutrient enrichment on Tridacna derasa seed: dissolved inorganic nitrogen increases growth rate. Aquaculture 106:41–49

    Article  CAS  Google Scholar 

  • Hawkins AJS, Klumpp DW (1995) Nutrition of the giant clam Tridacna gigas (L.). II. Relative contributions of filter-feeding and the ammonium–nitrogen acquired and recycled by symbiotic alga towards total nitrogen requirements for tissue growth and metabolism. J Exp Mar Bio Ecol 190:263–290

    Article  Google Scholar 

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

    Article  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

    Article  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. Physiol Rep. https://doi.org/10.14814/phy2.13209

    Article  PubMed  PubMed Central  Google Scholar 

  • Holm LM, Jahn TP, Møller ALB, Schjoerring JK, Ferri D, Klaerke DA, Zeuthen T (2005) NH3 and NH4 + permeability in aquaporin-expressing Xenopus oocytes. Pflug Arch 450:415–428

    Article  CAS  Google Scholar 

  • Ip YK, Chew SF (2010) Ammonia production, excretion, toxicity, and defense in fish: a review. Front Physiol. https://doi.org/10.3389/fphys.2010.00134

    Article  PubMed  PubMed Central  Google Scholar 

  • Ip YK, Ching B, Hiong KC, Choo CYL, Boo MV, Wong WP, Chew SF (2015) Light induces changes in activities of Na+/K+-ATPase, H+/K+-ATPase and glutamine synthetase in tissues involved directly or indirectly in light-enhanced calcification in the giant clam, Tridacna squamosa. Front Physiol 6:68. https://doi.org/10.3389/fphys.2015.00068

    Article  PubMed  PubMed Central  Google Scholar 

  • Ip YK, Hiong KC, Goh EJK, Boo MV, Choo CYL, Ching B, Wong WP, Chew SF (2017a) 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. https://doi.org/10.3389/fphys.2017.00781

    Article  PubMed  PubMed Central  Google Scholar 

  • Ip YK, Koh CZY, Hiong KC, Choo CYL, Boo MV, Wong WP, Neo ML, Chew SF (2017b) Carbonic Anhydrase 2-like in the giant clam, Tridacna squamosa: characterization, localization, response to light, and possible role in the transport of inorganic carbon from the host to its symbionts. Physiol Rep. https://doi.org/10.14814/phy2.13494

    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

    Article  PubMed  CAS  Google Scholar 

  • Javelle A, Lupo D, Zheng L, Li X, Winkler FK, Merrick M (2006) An unusual twin-His arrangement in the pore of ammonia channels is essential for substrate conductance. J Biol Chem 281:39492–39498

    Article  PubMed  CAS  Google Scholar 

  • Javelle A, Lupo D, Ripoche P, Fulford T, Merrick M, Winkler FK (2008) Substrate binding, deprotonation, and selectivity at the periplasmic entrance of the Escherichia coli ammonia channel AmtB. Proc Natl Acad Sci USA 105:5040–5045

    Article  PubMed  Google Scholar 

  • Khademi S, O’Connell J III, Remis J, Robles-Colmenares Y, Miercke LJ, Stroud RM (2004) Mechanism of ammonia transport by Amt/MEP/Rh: structure of AmtB at 1.35 A. Science 305:1587–1594

    Article  PubMed  CAS  Google Scholar 

  • Kirsten JH, Xiong Y, Davis CT, Singleton CK (2008) Subcellular localization of ammonium transporters in Dictyostelium discoideum. BMC Cell Biol. https://doi.org/10.1186/1471-2121-9-71

    Article  PubMed  PubMed Central  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

    Article  Google Scholar 

  • Klumpp DW, Bayne BL, Hawkins AJS (1992) Nutrition of the giant clam Tridacna gigas (L.). 1. Contribution of filter feeding and photosynthates to respiration and growth. J Exp Mar Biol Ecol 155:105–122

    Article  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. https://doi.org/10.3389/fphys.2018.00281

    Article  PubMed  PubMed Central  Google Scholar 

  • Larsen EH, Deaton LE, Onken H, O’Donnell M, Grosell M, Dantzler WH, Weihrauch D (2014) Osmoregulation and excretion. Comp Physiol 4:405–573

    Article  Google Scholar 

  • Lauter FR, Ninnemann O, Bucher M, Riesmeier JW, Frommer WB (1996) Preferential expression of an ammonium transporter and of two putative nitrate transporters in root hairs of tomato. Proc Natl Acad Sci USA 93:8139–8144

    Article  PubMed  CAS  Google Scholar 

  • Li T, Liao K, Xu X, Gao Y, Wang Z, Zhu X, Jia B, Xuan Y (2017) Wheat ammonium transporter (AMT) gene family: diversity and possible role in host–pathogen interaction with stem rust. Front Plant Sci. https://doi.org/10.3389/fpls.2017.01637

    Article  PubMed  PubMed Central  Google Scholar 

  • Loqué D, Lalonde S, Looger LL, von Wirén N, Frommer WB (2007) A cytosolic trans-activation domain essential for ammonium uptake. Nature 446:95–198

    Article  CAS  Google Scholar 

  • Lucas JS, Nash WJ, Crawford CM, Braley RD (1989) Environmental influences on growth and survival during the ocean-nursery rearing of giant clams, Tridacna gigas (L.). Aquaculture 80:45–61

    Article  Google Scholar 

  • Marcaggi P, Coles JA (2001) Ammonium in nervous tissue: transport across cell membranes, fluxes from neurons to glial cells, and role in signaling. ‎Prog Neurobiol 64:157–183

    Article  PubMed  CAS  Google Scholar 

  • Marini AM, Soussi-Boudekou S, Vissers S, Andre B (1997) A family of ammonium transporters in Saccharomyces cerevisiae. Mol Cell Biol 17:4282–4293

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Muscatine L (1990) The role of symbiotic algae in carbon and energy flux in reef corals. Coral Reefs 25:1–29

    Google Scholar 

  • Muscatine L, Falkowski PG, Dubinsky Z (1983) Carbon budgets in symbiotic associations. In: Schenk HEA, Schwemmler W (eds) Endocytobiology. de Gruyter, Berlin, pp 649–658

    Google Scholar 

  • Nakhoul NL, Hering-Smith KS, Abdulnour-Nakhoul SM, Hamm LL (2001) Transport of NH3/NH4 + in oocytes expressing aquaporin-1. Am J Physiol Renal Physiol 281:255–263

    Article  Google Scholar 

  • Neo ML, Wabnitz CCC, Braley RD, Heslinga GA, Fauvelot C, Van Wynsberge S, Andréfouët S, Waters C, Tan AS-H, Gomez ED, Costello MJ, Todd PA (2017) Giant clams (Bivalvia: Cardiidae: Tridacninae): a comprehensive update of species and their distribution, current threats and conservation status. Oceanogr Mar Biol 55:87–387, 2017

    Google Scholar 

  • Neuhäuser B, Dynowski M, Mayer M, Ludewig U (2007) Regulation of NH4 + transport by essential cross talk between AMT monomers through the carboxyl tails. Plant Physiol 143:1651–1659

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Norton JH, Shepherd MA, Long HM, Fitt WK (1992) The zooxanthellae tubular system in the giant clam. Biol Bull 183:503–506

    Article  PubMed  CAS  Google Scholar 

  • Onate JA, Naguit MRA (1989) A preliminary study on the effect of increased nitrate concentration on the growth of giant clams Hippopus hippopus. In: Zaragoza EC, de Guzman DL, Gonzales EP (eds) Culture of giant clams (Bivalvia:Tridacnidae). Australian Centre for International Agricultural Research, Canberra, pp 57–61

    Google Scholar 

  • Pantoja O (2012) High affinity ammonium transporters: molecular mechanism of action. Front Plant Sci. https://doi.org/10.3389/fpls.2012.00034

    Article  PubMed  PubMed Central  Google Scholar 

  • Peng J, Huang CH (2006) Rh proteins vs Amt proteins: an organismal and phylogenetic perspective on CO2 and NH3 gas channels. Transfus Clin Biol 13:85–94

    Article  PubMed  CAS  Google Scholar 

  • Rees TA, Fitt WK, Yellowlees D (1994) Host glutamine synthetase activities in the giant clam-zooxanthellae symbiosis: effects of clam size, elevated ammonia and continous darkness. Mar Biol 118:681-685

    Article  CAS  Google Scholar 

  • Rosewater J (1965) Indo-Pacific mollusca. The family Tridacnidae in the Indo-Pacific. Department of Mollusks, Academy of Natural Sciences of Philadelphia, Philadelphia

    Google Scholar 

  • Sano Y, Kobayashi S, Shirai K, Takahata N, Matsumoto K, Watanabe T, Sowa K, Iwai K (2012) Past daily light cycle recorded in the strontium/calcium ratios of giant clam shells. Nat Commun. https://doi.org/10.1038/ncomms1763

    Article  PubMed  Google Scholar 

  • Saparov SM, Liu K, Agre P, Pohl P (2007) Fast and selective ammonia transport by aquaporin-8. J Biol Chem 282:5296–5301

    Article  PubMed  CAS  Google Scholar 

  • Shepherd D, Leggat W, Rees TAV, Yellowlees D (1999) Ammonium, but not nitrate, stimulates an increase in glutamine concentration in the hemolymph of Tridacna gigas. Mar Biol 133:45–53

    Article  CAS  Google Scholar 

  • Søgaard R, Alsterfjord M, MacAulay N, Zeuthen T (2009) Ammonium ion transport by the AMT/Rh homolog TaAMT1;1 is stimulated by acidic pH. Pflug Arch. https://doi.org/10.1007/s00424-009-0665-z

    Article  Google Scholar 

  • Soupene E, He L, Yan D, Kustu S (1998) Ammonia acquisition in enteric bacteria: physiological role of the ammonium/methylammonium transport B (AmtB) protein. Proc Natl Acad Sci USA 95:7030–7034

    Article  PubMed  CAS  Google Scholar 

  • Soupene E, Lee H, Kustu S (2002) Ammonium/methylammonium transport (Amt) proteins facilitate diffusion of NH3 bidirectionally. Proc Natl Acad Sci USA 99:3926–3931

    Article  PubMed  CAS  Google Scholar 

  • Streamer M, Griffiths DJ, Luong-van Thinh (1988) The products of photosynthesis by zooxanthellae (Symbiodinium microadriaticum) of Tridacna gigas and their transfer to the host. Symbiosis 6:237–252

    CAS  Google Scholar 

  • Summons RE, Boag TS, Osmond CB (1986) The effect of ammonium on photosynthesis and the pathway of ammonium assimilation in Gymnodinium microadriaticum in vitro and in symbiosis with tridacnid clams and corals. Proc R Soc Lond B Biol Sci 227:147–159

    Article  CAS  Google Scholar 

  • Taylor L, Curthoys NP (2004) Glutamine metabolism: role in acid–base balance. Biochem Mol Biol Educ 32:291–304

    Article  PubMed  CAS  Google Scholar 

  • Thomas RC (1984) Experimental displacement of intracellular pH and the mechanism of its subsequent recovery. J Physiol Lond 354:3–22

    Article  Google Scholar 

  • Trench RK (1987) Dinoflagellates in non-parasitic symbiosis. In: Taylor FJR (ed) The biology of dinoflagellates. Blackwell Scientific, Oxford, pp 530–570

    Google Scholar 

  • Weihrauch D, Morris S, Towle DW (2004) Ammonia excretion in aquatic and terrestrial crabs. J Exp Biol 207:4491–4504

    Article  PubMed  CAS  Google Scholar 

  • Wilkerson FP, Trench RK (1986) Uptake of dissolved inorganic nitrogen by the symbiotic clam Tridacna gigas and the coral Acropora sp. Mar Biol 93:237–246

    Article  CAS  Google Scholar 

  • Wright PA (1995) Nitrogen excretion: three end products, many physiological roles. J Exp Biol 198:273–281

    PubMed  CAS  Google Scholar 

  • Wu X, Yang H, Qu C, Xu Z, Li W, Hao B, Yang C, Sun G, Liu G (2015) Sequence and expression analysis of the AMT gene family in poplar. Front Plant Sci. https://doi.org/10.3389/fpls.2015.00337

    Article  PubMed  PubMed Central  Google Scholar 

  • Yoshino R, Morio T, Yamada Y, Kuwayama H, Sameshima M, Tanaka Y, Sesaki H, Iijima M (2007) Regulation of ammonia homeostasis by the ammonium transporter AmtA in Dictyostelium discoideum. Eukaryot Cell 6:2419–2428

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yuan L, Loqué D, Kojima S, Rauch S, Ishiyama K, Inoue E, Takahashi H, von Wirén N (2007) The organization of high-affinity ammonium uptake in Arabidopsis roots depends on the spatial arrangement and biochemical properties of AMT1-type transporters. Plant Cell 19:2636–2652

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yuan L, Graff L, Loqué D, Kojima S, Tsuchiya YN, Takahashi H, von Wirén N (2009) AtAMT1;4, a pollen-specific high-affinity ammonium transporter of the plasma membrane in Arabidopsis. Plant Cell Physiol 50:13–25

    Article  PubMed  CAS  Google Scholar 

  • Zheng L, Kostrewa D, Bernèche S, Winkler FK, Li X (2004) The mechanism of ammonia transport based on the crystal structure of AmtB of Escherichia coli. Proc Natl Acad Sci USA 101:17090–17095

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This study was supported by the Singapore Ministry of Education through a Grant (R-154-000-A37-114) to Y. K. Ip.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, National University of Singapore, Kent Ridge, Singapore, 117543, Republic of Singapore

    Mel V. Boo, Kum C. Hiong, Enan J. K. Goh, Celine Y. L. Choo, Wai P. Wong & Yuen K. Ip

  2. The Tropical Marine Science Institute, National University of Singapore, Kent Ridge, Singapore, 119227, Republic of Singapore

    Yuen K. Ip

  3. Natural Sciences and Science Education, National Institute of Education, Nanyang Technological University, 1 Nanyang Walk, Singapore, 637616, Republic of Singapore

    Shit F. Chew

Authors
  1. Mel V. Boo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kum C. Hiong
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Enan J. K. Goh
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Celine Y. L. Choo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Wai P. Wong
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Shit F. Chew
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yuen K. Ip
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yuen K. Ip.

Ethics declarations

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Additional information

Communicated by I. D. Hume.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Boo, M.V., Hiong, K.C., Goh, E.J.K. et al. 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 (2018). https://doi.org/10.1007/s00360-018-1161-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-018-1161-6

Keywords

Search

Navigation