Skip to main content

Advertisement

Log in

Phototrophic potential and form II ribulose-1,5-bisphosphate carboxylase/oxygenase expression in five organs of the fluted giant clam, Tridacna squamosa

  • Report
  • Published:
Coral Reefs Aims and scope Submit manuscript

Abstract

Despite living in oligotrophic tropical waters, giant clams can grow to large sizes because they live in symbiosis with extracellular phototrophic dinoflagellates (zooxanthellae) and receive photosynthates from them. The physical presence of zooxanthellae in five organs (colorful outer mantle, whitish inner mantle, ctenidium, hepatopancreas and foot muscle) of Tridacna squamosa had been confirmed by microscopy, and high densities of zooxanthellae were detected in specific regions of the inner mantle and foot muscle. Symbiotic dinoflagellates use form II ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO) to fix inorganic carbon during C3 photosynthesis. Using qPCR primers that were designed comprehensively against all known zooxanthellal form II RuBisCO gene sequences (rbcII) in existing databases, we demonstrated that the outer mantle of T. squamosa (TS) had the greatest phototrophic potential as reflected by its high zooxanthellal rbcII (TSZrbcII) transcript level, which varied among different regions of the outer mantle. The other four organs also expressed moderate levels of TSZrbcII, despite the lack of iridophores and direct light exposure. Importantly, light exposure led to significant increases in the protein abundance of TSZRBCII in the outer mantle but not the other four organs. Taken together, these results indicate that organs inside the mantle cavity had low phototrophic potentials, but zooxanthellae residing inside these organs might serve some unidentified functions to benefit the host.

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

Access this article

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

Instant access to the full article PDF.

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

Similar content being viewed by others

References

  • Andréfouët S, Van Wynsberge Simon, Fauvelot C, Bruckner AW, Remoissenet G (2014) Significance of new records of Tridacna squamosa Lamarck, 1819, in the Tuamotu and Gambier Archipelagos (French Polynesia). Molluscan Res 34:277–284

    Google Scholar 

  • Aranda M, Li Y, Liew YJ, Baumgarten S, Simakov O, Wilson MC, Piel J, Ashoor H, Bougouffa S, Bajic VB, Ryu T, Ravasi T, Bayer T, Micklem G, Kim H, Bhak J, LaJeunesse TC, Voolstra CR (2016) Genomes of coral dinoflagellate symbionts highlight evolutionary adaptations conducive to a symbiotic lifestyle. Sci Rep 6:39734. https://doi.org/10.1038/srep39734

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Armstrong EJ, Roa JN, Stillman JH, Tresguerres M (2018) Symbiont photosynthesis in giant clams is promoted by V-type H+-ATPase from host cells. J Exp Biol 221:177220. https://doi.org/10.1242/jeb.177220

    Article  Google Scholar 

  • Bayer T, Aranda M, Sunagawa S, Yum LK, DeSalvo MK, Lindquist E, Coffroth MA, Voolstra CR, Medina M (2012) Symbiodinium transcriptomes: genome insights into the dinoflagellate symbionts of reef-building corals. PLoS ONE 7:e35269. https://doi.org/10.1371/journal.pone.0035269

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carty S (2003) Dinoflagellates. In: Wehr JD, Sheath RG (eds) Freshwater algae of North America: ecology and classification. Academic Press, San Diego, pp 685–714

    Google Scholar 

  • Carty S, Parrow MW (2015) Dinoflagellates. In: Wehr JD, Sheath RG, Kociolek JP (eds) Freshwater algae of North America: ecology and classification, 2nd edn. Academic Press, San Diego, USA, pp 773–807

    Google Scholar 

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

    PubMed  Google Scholar 

  • Erb TJ, Zarzycki J (2018) A short history of RubisCO: the rise and fall (?) of Nature’s predominant CO2 fixing enzyme. Curr Opin Biotech 49:100–107

    CAS  PubMed  Google Scholar 

  • Fine M, Sabbah S, Shashar N, Hoegh-Guldberg O (2013) Light from down under. J Exp Biol 216:4341–4346

    PubMed  Google Scholar 

  • Fisher CR, Fitt WK, Trench RK (1985) Photosynthesis and respiration in Tridacna gigas as a function of irradiance and size. Biol Bull 169:230–245

    Google Scholar 

  • Füssy Z, Faitová T, Oborník M (2019) Subcellular compartments interplay for carbon and nitrogen allocation in Chromera velia and Vitrella brassicaformis. Genome Biol Evol 11:1765–1779

    PubMed  PubMed Central  Google Scholar 

  • Grasso CR (2015) Investigating the effects of high light versus low light in two different types of Symbiodinium within the reef-building coral, Acropora millepora. Ph.D. thesis, University of Delaware

  • Griffiths DJ, Winsor H, Luongvan T (1992) Iridophores in the mantle of giant clams. Aust J Zool 40:319–326

    Google Scholar 

  • Heldt H, Piechulla B (2011) A leaf cell consists of several metabolic compartments. In: Plant biochemistry, 4th edn. Academic Press, San Diego, pp 1–42

    Google Scholar 

  • Hernawan UE (2008) Review: symbiosis between the giant clams (Bivalvia: Cardiidae) and zooxanthellae (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. Physiol Rep 5:e13209. https://doi.org/10.14814/phy2.13209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holt AL, Vahidinia S, Gagnon YL, Morse DE, Sweeney AM (2014) Photosymbiotic giant clams are transformers of solar flux. J Roy Soc Interface 11:20140678. https://doi.org/10.1098/rsif.2014.0678

    Article  Google Scholar 

  • Ikeda S, Yamashita H, Kondo S, Inoue K, Morishima S, Koike K (2017) Zooxanthellal genetic varieties in giant clams are partially determined by species-intrinsic and growth-related characteristics. PLoS ONE 12:e0172285. https://doi.org/10.1371/journal.pone.0172285

    Article  CAS  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 8:781. 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 5:e13494. https://doi.org/10.14814/phy2.13494

    Article  CAS  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

    CAS  PubMed  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 

  • Jones RJ, Hoegh-Guldberg O (2001) Diurnal changes in the photochemical efficiency of the symbiotic dinoflagellates (Dinophyceae) of corals: photoprotection, photoinactivation and the relationship to coral bleaching. Plant Cell Environ 24:89–99

    CAS  Google Scholar 

  • Juinio MAR, Menez LAB, Villanoy CL, Gomez ED (1989) Status of giant clam resources of the Philippines. J Molluscan Stud 55:431–440

    Google Scholar 

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

    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 

  • Kowalewska L, Mazur R, Suski S, Garstka M, Mostowska A (2016) Three-dimensional visualization of the tubular-lamellar transformation of the internal plastid membrane network during runner bean chloroplast biogenesis. Plant Cell 28:875–891

    CAS  PubMed  PubMed Central  Google Scholar 

  • LaJeunesse TC, Bhagooli R, Hidaka M, DeVantier L, Done T, Schmidt GW, Fitt WK, Hoegh-Guldberg O (2004) Closely related Symbiodinium spp. differ in relative dominance in coral reef host communities across environmental, latitudinal and biogeographic gradients. Mar Ecol Prog Ser 284:147–161

    Google Scholar 

  • LaJeunesse TC, Parkinson JE, Gabrielson PW, Jeong HJ, Reimer JD, Voolstra CR, Santos SR (2018) Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr Biol 28:2570–2580

    CAS  PubMed  Google Scholar 

  • Lee SY, Jeong HJ, Kang NS, Jang TY, Jang SH, Lajeunesse TC (2015) Symbiodinium tridacnidorum sp. nov., a dinoflagellate common to Indo-Pacific giant clams, and a revised morphological description of Symbiodinium microadriaticum Freudenthal, emended Trench & Blank. Eur J Phycol 50:155–172

    Google Scholar 

  • Leggat W, Buck BH, Grice A, Yellowlees D (2003) The impact of bleaching on the metabolic contribution of dinoflagellate symbionts to their giant clam host. Plant Cell Environ 26:1951–1961

    CAS  Google Scholar 

  • Levin RA, Beltran VH, Hill R, Kjelleberg S, Mcdougald D, Steinberg PD, van Oppen MJH (2016) Sex, scavengers, and chaperones: transcriptome secrets of divergent Symbiodinium thermal tolerances. Mol Biol Evol 33:2201–2215

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liew YJ, Aranda M, Voolstra CR (2016) Reefgenomics.Org—a repository for marine genomics data. Database 2016:baw152. https://doi.org/10.1093/database/baw152

    Article  PubMed  PubMed Central  Google Scholar 

  • Marra J (1978) Effect of short-term variations in light intensity on photosynthesis of a marine phytoplankter: a laboratory simulation study. Mar Biol 46:191–202

    CAS  Google Scholar 

  • Mayfield AB, Hsiao YY, Chen HK, Chen CS (2014) Rubisco expression in the dinoflagellate Symbiodinium sp. is influenced by both photoperiod and endosymbiotic lifestyle. Mar Biotechnol 16:371–384

    CAS  PubMed  Google Scholar 

  • McFarland WN, Munz FW (1975) Part II: the photic environment of clear tropical seas during the day. Vision Res 15:1063–1070

    CAS  PubMed  Google Scholar 

  • Morse D, Salois P, Markovic P, Hastings JW (1995) A nuclear-encoded form II RuBisCO in dinoflagellates. Science 268:1622–1624

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Pichard SL, Campbell L, Kang JB, Tabita FR, Paul JH (1996) Regulation of ribulose bisphosphate carboxylase expression in natural phytoplankton communities. I. Diel rhythms. Mar Ecol Prog Ser 139:257–265

    CAS  Google Scholar 

  • Plöscher M, Reisinger V, Eichacker LA (2011) Proteomic comparison of etioplast and chloroplast protein complexes. J Proteom 74:1256–1265

    Google Scholar 

  • Rosic N, Yew ESL, Chan CKK, Lee HC, Kaniewska P, Edwards D, Dove S, Hoegh-Guldberg O (2015) Unfolding the secrets of coral–algal symbiosis. ISME J 9:844–856

    CAS  PubMed  Google Scholar 

  • Rouzé H, Hédouin L (2018) Bilateral asymmetry in bleaching susceptibility within a giant clam, Tridacna maxima. Coral Reefs 37:825

    Google Scholar 

  • Rowan R, Whitney SM, Fowler A, Yellowlees D (1996) Rubisco in marine symbiotic dinoflagellates: form II enzymes in eukaryotic oxygenic phototrophs encoded by a nuclear multigene family. Plant Cell 8:539–553

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ryther JH (1956) Photosynthesis in the ocean as a function of light intensity. Limnol Oceanogr 1:61–70

    Google Scholar 

  • Sadali NM, Sowden RG, Ling Q, Jarvis RP (2019) Differentiation of chromoplasts and other plastids in plants. Plant Cell Rep 38:803–818

    CAS  PubMed  PubMed Central  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 3:761. https://doi.org/10.1038/ncomms1763

    Article  CAS  PubMed  Google Scholar 

  • Shoguchi E, Beedessee G, Tada I, Hisata K, Kawashima T, Takeuchi T, Arakaki N, Fujie M, Koyanagi R, Roy MC, Kawachi M, Hidaka M, Satoh N, Shinzato C (2018) Two divergent Symbiodinium genomes reveal conservation of a gene cluster for sunscreen biosynthesis and recently lost genes. BMC Genomics 19:458. https://doi.org/10.1186/s12864-018-4857-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Solymosi K, Schoefs B (2010) Etioplast and etio-chloroplast formation under natural conditions: the dark side of chlorophyll biosynthesis in angiosperms. Photosynth Res 105:143–166

    CAS  PubMed  Google Scholar 

  • Streamer M, McNeil YR, Yellowlees D (1993) Photosynthetic carbon dioxide fixation in zooxanthellae. Mar Biol 115:195–198

    CAS  Google Scholar 

  • Sui X, Mao S, Wang L, Zhang B, Zhang Z (2012) Effect of low light on the characteristics of photosynthesis and chlorophyll a fluorescence during leaf development of sweet pepper. J Integr Agr 11:1633–1643

    CAS  Google Scholar 

  • Tabita FR, Satagopan S, Hanson TE, Kreel NE, Scott SS (2008) Distinct form I, II, III, and IV Rubisco proteins from the three kingdoms of life provide clues about Rubisco evolution and structure/function relationships. J Exp Bot 59:1515–1524

    CAS  PubMed  Google Scholar 

  • Takabayashi M, Santos SR, Cook CB (2004) Mitochondrial DNA phylogeny of the symbiotic dinoflagellates (Symbiodinium, Dinophyta). J Phycol 40:160–164

    CAS  Google Scholar 

  • Thorrez L, Van Deun K, Tranchevent L-C, Van Lommel L, Engelen K, Marchal K, Moreau Y, Van Mechelen I, Schuit F (2008) Using ribosomal protein genes as reference: a tale of caution. PLoS ONE 3:e1854. https://doi.org/10.1371/journal.pone.0001854

    Article  CAS  PubMed  PubMed Central  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 

  • van Dooren GG, Striepen B (2013) The algal past and parasite present of the apicoplast. Annu Rev Microbiol 67:271–289

    PubMed  Google Scholar 

  • van Dooren GG, Hapuarachchi SV (2017) The dark side of the chloroplast: biogenesis, metabolism and membrane biology of the apicoplast. Adv Bot Res 84:145–185

    Google Scholar 

  • Weber M (2009) The biogeography and evolution of Symbiodinium in giant clams (Tridacnidae). Ph.D. thesis, University of California

  • Wells SM, Barzdo JG (1991) International trade in marine species: Is CITES a useful control mechanism? Coast Manage 19:135–154

    Google Scholar 

  • Whitney SM, Yellowlees D (1995) Preliminary investigations into the structure and activity of ribulose bisphosphate carboxylase from two photosynthetic dinoflagellates. J Phycol 31:138–146

    CAS  Google Scholar 

  • Zhu M, Lin J, Ye J, Wang R, Yang C, Gong J, Liu Y, Deng C, Liu P, Chen C, Cheng Y, Deng X, Zeng Y (2018) A comprehensive proteomic analysis of elaioplasts from citrus fruits reveals insights into elaioplast biogenesis and function. Hortic Res 5:6. https://doi.org/10.1038/s41438-017-0014-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zinser ER, Lindell D, Johnson ZI, Futschik ME, Steglich C, Coleman ML, Wright MA, Rector T, Steen R, McNulty N, Thompson LR, Chisholm SW (2009) Choreography of the transcriptome, photophysiology, and cell cycle of a minimal photoautotroph, Prochlorococcus. PLoS ONE 4:e5135. https://doi.org/10.1371/journal.pone.0005135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This study was supported by the Singapore Ministry of Education through Grants (R-154-000-A37-114 and R‐154‐000‐B69-114) to Ip YK.

Author information

Authors and Affiliations

Authors

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

Institutional approval was not required for research on giant clams (National University of Singapore Institutional Animal Care and Use Committee). Nonetheless, all applicable international, national and/or institutional guidelines for the care and use of animals were followed.

Additional information

Topic Editor Simon Davy

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 2548 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Poo, J.S.T., Choo, C.Y.L., Hiong, K.C. et al. 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 (2020). https://doi.org/10.1007/s00338-020-01898-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-020-01898-7

Keywords

Navigation