Skip to main content

Cell Biology of Reef-Building Corals: Ion Transport, Acid/Base Regulation, and Energy Metabolism

  • Chapter
  • First Online:
Acid-Base Balance and Nitrogen Excretion in Invertebrates

Abstract

Coral reefs are built by colonial cnidarians that establish a symbiotic relationship with dinoflagellate algae of the genus Symbiodinium. The processes of photosynthesis, calcification, and general metabolism require the transport of diverse ions across several cellular membranes and generate waste products that induce acid/base and oxidative stress. This chapter reviews the current knowledge on coral cell biology with a focus on ion transport and acid/base regulation while also discussing related aspects of coral energy metabolism.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 39.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 54.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 54.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Agostini S, Suzuki Y, Higuchi T, Casareto BE, Yoshinaga K, Nakano Y, Fujimura H (2011) Biological and chemical characteristics of the coral gastric cavity. Coral Reefs 31:147–156

    Article  Google Scholar 

  • Al-Horani FA, Al-Moghrabi AM, De Beer D (2003) Microsensor study of photosynthesis and calcification in the scleractinian coral, Galaxea fascicularis: active internal carbon cycle. J Exp Mar Biol Ecol 288:1–15

    Article  Google Scholar 

  • Albright R, Mason B, Miller M, Langdon C (2010) Ocean acidification compromises recruitment success of the threatened Caribbean coral Acropora palmata. Proc Natl Acad Sci U S A 107:20400–20404

    Google Scholar 

  • Alieva NO, Konzen KA, Field SF, Meleshkevitch EA, Hunt ME, Beltran-Ramirez V, Miller DJ, Wiedenmann J, Salih A, Matz MV (2008) Diversity and evolution of coral fluorescent proteins. PLoS One 3(7):e2680. doi:10.1371/journal.pone.0002680

  • Allemand D, Furla P, Bénazet-Tambutté S (1998) Mechanisms of carbon acquisition for endosymbiont photosynthesis in Anthozoa. Can J Bot 76:925–941

    CAS  Google Scholar 

  • Allemand D, Ferrier-Pagès C, Furla P, Houlbrèque F, Puverel S, Reynaud S, Tambutté E, Tambutté S, Zoccola D (2004) Biomineralisation in reef-building corals: from molecular mechanisms to environmental control. Comptes Rendus Palevol 3:453–467

    Google Scholar 

  • Allemand D, Tambutté E, Zoccola D, Tambutté S (2011) Coral calcification, cells to reefs. In: Dubinsky Z, Stambler N (eds) Coral reefs an ecosystem in transition. Springer, New York, pp 119–150

    Chapter  Google Scholar 

  • Allison N, Cohen I, Finch AA, Erez J, Tudhope AW, Edinburgh Ion Microprobe Facility (2014) Corals concentrate dissolved inorganic carbon to facilitate calcification. Nat Commun 5:5741

    Article  PubMed  CAS  Google Scholar 

  • Andersson AJ, Gledhill D (2013) Ocean acidification and coral reefs: effects on breakdown, dissolution, and net ecosystem calcification. Ann Rev Mar Sci 5:321–348

    Article  PubMed  Google Scholar 

  • Andersson AJ, Kline DI, Edmunds PJ, Archer SD, Bednaršek N, Carpenter RC, Chadsey M, Goldstein P, Grottoli AG, Hurst TP et al (2015) Understanding ocean acidification impacts on organismal to ecological scales. Oceanography 28:16–27

    Article  Google Scholar 

  • Anthony KR, Kline DI, Diaz-Pulido G, Dove S, Hoegh-Guldberg O (2008) Ocean acidification causes bleaching and productivity loss in coral reef builders. Proc Natl Acad Sci U S A 105:17442–17446

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Babcock RC, Heyward AJ (1986) Larval development of certain gamete-spawning scleractinian corals. Coral Reefs 5:111–116

    Article  Google Scholar 

  • Barott KL, Helman Y, Haramaty L, Barron ME, Hess KC, Buck J, Levin LR, Tresguerres M (2013) High adenylyl cyclase activity and in vivo cAMP fluctuations in corals suggest central physiological role. Sci Rep 3:1–7

    Article  CAS  Google Scholar 

  • Barott KL, Perez SO, Linsmayer LB, Tresguerres M (2015a) 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:R235–R246

    Article  PubMed  CAS  Google Scholar 

  • Barott KL, Venn AA, Perez SO, Tambutté S, Tresguerres M (2015b) Coral host cells acidify symbiotic algal microenvironment to promote photosynthesis. Proc Natl Acad Sci U S A 112:607–612

    Article  PubMed  CAS  Google Scholar 

  • Bates NR, Amat A, Andersson A (2010) Feedbacks and responses of coral calcification on the Bermuda reef system to seasonal changes in biological processes and ocean acidification. Biogeosciences 7:2509–2530

    Article  CAS  Google Scholar 

  • Beerling DJ, Royer DL (2011) Convergent Cenozoic CO2 history. Nat Geosci 4:418–420

    Article  CAS  Google Scholar 

  • Ben-Zvi O, Eyal G, Loya Y (2015) Light-dependent fluorescence in the coral Galaxea fascicularis. Hydrobiologia 759:15–26

    Article  Google Scholar 

  • Benson AA, Patton JS, Abraham S (1978) Energy exchange in coral reef ecosystems. Atoll Res Bull 220:33–54

    Article  Google Scholar 

  • Bertucci A, Tambutté E, Tambutté S, Allemand D, Zoccola D (2010) Symbiosis-dependent gene expression in coral-dinoflagellate association: cloning and characterization of a P-type H+ −ATPase gene. Proc Biol Sci 277:87–95

    Google Scholar 

  • Bindoff NL, Willebrand J, Artale V, Cazenave A, Gregory J, Gulev S (2007) Observations: oceanic climate change and sea level. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt K, Tignor M (eds) Climate change 2007: the physical science basis contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, New York

    Google Scholar 

  • Bomati EK, Manning G, Deheyn DD (2009) Amphioxus encodes the largest known family of green fluorescent proteins, which have diversified into distinct functional classes. BMC Evol Biol 9:1–11

    Google Scholar 

  • Bou-Abdallah F, Chasteen ND, Lesser MP (2006) Quenching of superoxide radicals by green fluorescent protein. Biochim Biophys Acta Gen Subj 1760(11):1690–1695

    Google Scholar 

  • Bourne GC (1900) The anthozoa. In: Lankester ER (ed) A treatise on zoology. Part II. The porifera and coelenterata. Adam & Charles Black, London, pp 1–84

    Google Scholar 

  • Buck J, Sinclair ML, Schapal L, Cann MJ, Levin LR (1999) Cytosolic adenylyl cyclase defines a unique signaling molecule in mammals. Proc Natl Acad Sci 96:79–84

    Google Scholar 

  • Burke L, Reytar K, Spalding M, Perry A (2011) Reefs at risk revisited. World Resources Institute, Washington, DC

    Google Scholar 

  • Burriesci MS, Raab TK, Pringle JR (2012) Evidence that glucose is the major transferred metabolite in dinoflagellate-cnidarian symbiosis. J Exp Biol 215:3467–3477

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Caldeira K, Wickett ME (2003) Oceanography: anthropogenic carbon and ocean pH. Nature 425:365

    Article  PubMed  CAS  Google Scholar 

  • Castillo KD, Ries JB, Bruno JF, Westfield IT (2014) The reef-building coral Siderastrea siderea exhibits parabolic responses to ocean acidification and warming. Proc R Soc B Biol Sci 281:20141856

    Google Scholar 

  • Catala-Stucki R (1959) Fluorescent effects from corals irradiated with ultra-violet rays. Nature 183:949

    Article  Google Scholar 

  • Chalker BE, Taylor DL (1975) Light-enhanced calcification, and the role of oxidative phosphorylation in calcification of the coral Acropora cervicornis. Proc R Soc B Biol Sci 190:323–331

    Article  CAS  Google Scholar 

  • Chen Y, Cann MJ, Litvin TN, Iourgenko V, Sinclair ML, Levin LR, Buck J (2000) Soluble adenylyl cyclase as an evolutionarily conserved bicarbonate sensor. Science 289:625–628

    Google Scholar 

  • Chimetto LA, Brocchi M, Thompson CC, Martins RC, Ramos HR, Thompson FL (2008) Vibrios dominate as culturable nitrogen-fixing bacteria of the Brazilian coral Mussismilia hispida. Syst Appl Microbiol 31:312–319

    Article  PubMed  CAS  Google Scholar 

  • Clode PL, Marshall AT (2002) Low temperature FESEM of the calcifying interface of a scleractinian coral. Tissue Cell 34:187–198

    Article  PubMed  CAS  Google Scholar 

  • Cohen A, Holcomb M (2009) Why corals care about ocean acidification. Oceanography 22:118–127

    Article  Google Scholar 

  • Cohen AL, McConnaughey TA (2003) Geochemical perspectives on coral mineralization. Rev Mineral Geochem 54:151–187

    Google Scholar 

  • Crossland CJ, Barnes DJ, Borowitzka MA (1980) Diurnal lipid and mucus production in the staghorn coral Acropora acuminata. Mar Biol 60:81–90

    Article  CAS  Google Scholar 

  • Cunning R, Silverstein RN, Baker AC (2015a) Investigating the causes and consequences of symbiont shuffling in a multi-partner reef coral symbiosis under environmental change. Proc Biol Sci 282:20141725

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cunning R, Vaughan N, Gillette P, Capo TR, Matté JL, Baker AC (2015b) Dynamic regulation of partner abundance mediates response of reef coral symbioses to environmental change. Ecology 96:1411–1420

    Article  PubMed  CAS  Google Scholar 

  • Davies PS (1984) The role of zooxanthellae in the nutritional energy requirements of Pocillopora eydouxi. Coral Reefs 2:181–186

    Google Scholar 

  • Davy SK, Allemand D, Weis VM (2012) Cell biology of cnidarian-dinoflagellate symbiosis. Microbiol Mol Biol Rev 76:229–261

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dawson TL (2007) Light-harvesting and light-protecting pigments in simple life forms. Color Technol 123:129–142

    Article  CAS  Google Scholar 

  • Diekmann O, Bak R, Stam W, Olsen J (2001) Molecular genetic evidence for probable reticulate speciation in the coral genus Madracis from a Caribbean fringing reef slope. Mar Biol 139:221–233

    Article  CAS  Google Scholar 

  • Dove SG, Takabayashi M, Hoegh-Guldberg O (1995) Isolation and partial characterization of the pink and blue pigments of Pocilloporid and Acroporid corals. Biol Bull 189(3):288–297

    Google Scholar 

  • Dove SG, Hoegh-Guldberg O, Ranganathan S (2001) Major colour patterns of reef-building corals are due to a family of GFP-like proteins. Coral Reefs 19(3):197–204

    Google Scholar 

  • Dove SG, Lovell C, Fine M, Deckenback J, Hoegh-Guldberg O, Iglesias-Prieto R, Anthony KR (2008) Host pigments: potential facilitators of photosynthesis in coral symbioses. Plant Cell Environ 3:1523–1533

    Article  CAS  Google Scholar 

  • Drake JL, Mass T, Haramaty L, Zelzion E, Bhattacharya D, Falkowski PG (2014) Proteomic analysis of skeletal organic matrix from the stony coral Stylophora pistillata. Proc Natl Acad Sci 111:12728–12733

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ducklow HW, Mitchell R (1979) Composition of mucus released by coral reef coelenterates. Limnol Oceanogr 24:706–714

    Article  CAS  Google Scholar 

  • Dufault AM, Cumbo VR, Fan T-Y, Edmunds PJ (2012) Effects of diurnally oscillating pCO2 on the calcification and survival of coral recruits. Proc Biol Sci 279:2951–2958

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Erez J (1978) Vital effect on stable-isotope composition seen in foraminifera and coral skeletons. Nature 273:199–202

    Article  CAS  Google Scholar 

  • Fabricius KE, Langdon C, Uthike S, Humphrey C, Noonan S, Death G, Okazaki R, Muehllehner N, Glas MS, Lough JM (2011) Losers and winners in coral reefs acclimated to elevated carbon dioxide concentrations. Nat Clim Chang 1:165–169

    Article  CAS  Google Scholar 

  • Falkowski PG, Dubinsky Z, Muscatine L, Porter JW (1984) Light and bioenergetics of a symbiotic coral. BioScience 34:705–709

    Article  CAS  Google Scholar 

  • Farrell J, Ramos L, Tresguerres M, Kamenetsky M, Levin LR, Buck J (2008) Somatic ‘soluble’ Adenylyl Cyclase isoforms are unaffected in Sacytm1Lex/Sacytm1Lex ‘knockout’ mice. PLoS One 3:e3251

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Feely RA, Sabine CL, Lee K, Berelson W, Kleypas J, Fabry VJ, Millero FJ (2004) Impact of anthropogenic CO2 on the CaCO3 system in the oceans. Science 305:362–366

    Article  PubMed  CAS  Google Scholar 

  • Friedman PA, Gesek FA (1995) Cellular calcium transport in renal epithelia: measurement, mechanisms, and regulation. Physiol Rev 75:429–471

    Google Scholar 

  • Fukami H, Budd AF, Paulay G, Solé-Cava A, Allen Chen C, Iwao K, Knowlton N (2004) Conventional taxonomy obscures deep divergence between Pacific and Atlantic corals. Nature 427:832–835

    Article  PubMed  CAS  Google Scholar 

  • Furla P, Bénazet-Tambutté S, Jaubert J, Allemand D (1998) Functional polarity of the tentacle of the sea anemone Anemonia viridis: role in inorganic carbon acquisition. AJP: Regul Integr Comp Physiol 274:303–310

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Galloway SB, Work TM, Bochsler VS, Harley RA, Kramarsky-Winters E, McLaughlin SM, Meteyer CU, Morado JF, Nicholson JH, Parnell PG et al (2006) Coral disease and health workshop: coral histopathology II. National Oceanic and Atmospheric Administration (NOAA), Silver Spring

    Google Scholar 

  • Ganot P, Zoccola D, Tambutté E, Voolstra CR, Aranda M, Allemand D, Tambutté S (2015) Structural molecular components of septate junctions in cnidarians point to the origin of epithelial junctions in eukaryotes. Mol Biol Evol 32:44–62

    Article  PubMed  CAS  Google Scholar 

  • Gattuso JP (1999) Photosynthesis and calcification at cellular, organismal and community levels in coral reefs: a review on interactions and control by carbonate chemistry. Am Zool 39:160–183

    Article  CAS  Google Scholar 

  • Gattuso JP, Hendriks IE, Brewer PG (2014) Free-ocean CO2 enrichment (FOCE) systems: present status and future developments. Biogeosciences 11:4057–4075

    Article  CAS  Google Scholar 

  • Geng W, Wang Z, Zhang J, Reed BY, Pak CY, Moe OW (2005) Cloning and characterization of the human soluble adenylyl cyclase. AJP: Cell Physiol 288:C1305–C1316

    CAS  Google Scholar 

  • Gibbin EM, Putnam HM, Davy SK, Gates RD (2014) Intracellular pH and its response to CO2-driven seawater acidification in symbiotic versus non-symbiotic coral cells. J Exp Biol 217:1963–1969

    Article  PubMed  CAS  Google Scholar 

  • Gladfelter EH (1983) Circulation of fluids in the gastrovascular system of the reef coral Acropora cervicornis. Biol Bull 165:619–636

    Article  Google Scholar 

  • Goldberg WM (2001a) Acid polysaccharides in the skeletal matrix and calicoblastic epithelium of the stony coral Mycetophyllia reesi. Tissue Cell 33:376–387

    Article  PubMed  CAS  Google Scholar 

  • Goldberg WM (2001b) Desmocytes in the calicoblastic epithelium of the stony coral Mycetophyllia reesi and their attachment to the skeleton. Tissue Cell 33:388–394

    Article  PubMed  CAS  Google Scholar 

  • Goldberg WM (2002a) Feeding behavior, epidermal structure and mucus cytochemistry of the scleractinian Mycetophyllia reesi, a coral without tentacles. Tissue Cell 34:232–245

    Article  PubMed  Google Scholar 

  • Goldberg WM (2002b) Gastrodermal structure and feeding responses in the scleractinian Mycetophyllia reesi, a coral with novel digestive filaments. Tissue Cell 34:246–261

    Article  PubMed  Google Scholar 

  • Goreau TF (1959) The physiology of skeleton formation in corals. I. A method for measuring the rate of calcium deposition by corals under different conditions. Biol Bull 116:59–75

    Article  CAS  Google Scholar 

  • Goreau TF, Goreau NI (1959) The physiology of skeleton formation in corals. II. Calcium deposition by hermatypic corals under various conditions in the reef. Biol Bull 117:239–250

    Article  CAS  Google Scholar 

  • Goreau TF, Goreau NI, Yonge CM (1971) Reef corals: autotrophs or heterotrophs? Biol Bull 141:247–260

    Article  Google Scholar 

  • Haas AF, Smith JE, Thompson M, Deheyn DD (2014) Effects of reduced dissolved oxygen concentrations on physiology and fluorescence of hermatypic corals and benthic algae. Peer J 2:e235. doi:10.7717/peerj.235

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Haddock SHD, Moline MA, Case JF (2009) Bioluminescence in the sea. 2:443–493. http://dx.doi.org/10.1146/annurev-marine-120308-081028

  • Hall-Spencer JM, Rodolfo-Metalpa R, Martin S, Ransome E, Fine M, Turner SM, Rowley SJ, Tedesco D, Buia M-C (2008) Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 454:96–99

    Article  PubMed  CAS  Google Scholar 

  • Hanson MR, Kohler RH (2001) GFP imaging: methodology and application to investigate cellular compartmentation in plants. J Exp Bot 52(356):529–539

    Google Scholar 

  • Hess KC, Jones BH, Marquez B, Chen Y, Ord TS, Kamenetsky M, Miyamoto C, Zippin JH, Kopf GS, Suarez SS et al (2005) The “soluble” adenylyl cyclase in sperm mediates multiple signaling events required for fertilization. Dev Cell 9:249–259

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hosey MM, Lazdunski M (1988) Calcium channels: molecular pharmacology, structure and regulation. J Membr Biol 104:81–105

    Article  PubMed  CAS  Google Scholar 

  • Hughes AD, Grottoli AG, Pease TK, Matsui Y (2010) Acquisition and assimilation of carbon in non-bleached and bleached corals. Mar Ecol Prog Ser 420:91–101

    Article  CAS  Google Scholar 

  • Ip YK, Lim ALL, Lim RW (1991) Some properties of calcium activated adenosine triphosphatase from the hermatypic coral Galaxea fascicularis. Mar Biol 111:191–197

    Article  CAS  Google Scholar 

  • Isa Y (1986) An electron microscope study on the mineralization of the skeleton of the staghorn coral Acropora hebes. Mar Biol 93:91–101

    Article  CAS  Google Scholar 

  • Johnston IS (1980) The ultrastructure of skeletogenesis in hermatypic corals. Int Rev Cytol 67:171–214

    Article  CAS  Google Scholar 

  • Jokiel P (2011a) The reef coral two compartment proton flux model: a new approach relating tissue-level physiological processes to gross corallum morphology. J Exp Mar Biol Ecol 409:1–12

    Article  CAS  Google Scholar 

  • Jokiel PL (2011b) Ocean acidification and control of reef coral calcification by boundary layer limitation of proton flux. Bull Mar Sci 87:639–657

    Article  Google Scholar 

  • Jokiel PL (2013) Coral reef calcification: carbonate, bicarbonate and proton flux under conditions of increasing ocean acidification. Proc Biol Sci 280:20130031

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kaniewska P, Campbell PR, Kline DI, Rodriguez-Lanetty M, Miller DJ, Dove S, Hoegh-Guldberg O (2012) Major cellular and physiological impacts of ocean acidification on a reef building coral. PLoS One 7:e34659

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Karako-Lampert S, Zoccola D, Salmon-Divon M, Katzenellenbogen M, Tambutté S, Bertucci A, Hoegh-Guldberg O, Deleury E, Allemand D, Levy O (2014) Transcriptome analysis of the scleractinian coral Stylophora pistillata. PLoS One 9:e88615

    Google Scholar 

  • Kawaguti S (1937) On the physiology of reef corals. II. The effect of light on color and form of reefs. Palao Trop Biol Stat Stud 2:199–208

    Google Scholar 

  • Kawaguti S (1969) The effect of green fluorescent pigment on the productivity of the reef corals. Micronesica 5:313

    Google Scholar 

  • Kawaguti S, Sakumoto D (1948) The effect of light on the calcium deposition of corals. Bul Oceanogr Inst Taiwan 4:65–70

    Google Scholar 

  • Kelmanson IV, Matz MV (2003) Molecular basis and evolutionary origins of color diversity in great star coral Montastraea cavernosa (Scleractinia: Faviida). Mol Biol Evol 20(7):1125–1133

    Google Scholar 

  • Kenkel CD, Traylor MR, Wiedenmann J, Salih A, Matz MV (2011) Fluorescence of coral larvae predicts their settlement response to crustose coralline algae and reflects stress. Proc Biol Sci 278:2691–2697

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kleypas J, Langdon C (2006) Coral reefs and changing seawater carbonate chemistry. In: Phinney JT, Hoegh-Guldberg O, Kleypas J, Skirving W, Strong A (eds) Coral reefs and climate change science and management. American Geophysical Union, Washington, DC

    Google Scholar 

  • Kline DI, Teneva L, Hauri C, Schneider K, Miard T, Chai A, Marker M, Dunbar R, Caldeira K, Lazar B et al (2015) Six month in situ high-resolution carbonate chemistry and temperature study on a coral reef flat reveals asynchronous pH and temperature anomalies. PLoS One 10:e0127648

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kline DI, Teneva L, Schneider K, Miard T, Chai A, Marker M, Headley K, Opdyke B, Nash M, Valetich M et al (2012) A short-term in situ CO2 enrichment experiment on Heron Island (GBR). Sci Rep 2:413

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Krediet CJ, Ritchie KB, Paul VJ, Teplitski M (2013) Coral-associated micro-organisms and their roles in promoting coral health and thwarting diseases. Proc Biol Sci 280:20122328

    Article  PubMed  PubMed Central  Google Scholar 

  • Kroeker KJ, Kordas RL, Crim RN, Singh GG (2010) Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecol Lett 13:1419–1434

    Article  PubMed  Google Scholar 

  • Kroeker KJ, Micheli F, Gambi MC (2013) Ocean acidification causes ecosystem shifts via altered competitive interactions. Nat Clim Chang 3:156–159

    Article  CAS  Google Scholar 

  • Kühl M, Cohen Y, Dalsgaard T, Jorgensen BB, Revbech NP (1995) Microenvironment and photosynthesis of zooxanthellae in scleractinian corals studied with microsensors for O2, pH and light. Mar Ecol Prog Ser 117:159–172

    Google Scholar 

  • Labas YA, Gurskaya NG, Yanushevich YG, Fradkov AF, Lukyanov KA, Lukyanov SA, Matz MV (2002) Diversity and evolution of the green fluorescent protein family. Proc Natl Acad Sci U S A 99(7):4256–4261

    Google Scholar 

  • Langdon C, Atkinson MJ (2005) Effect of elevated pCO2 on photosynthesis and calcification on corals and interactions with seasonal change in temperature/irradiance and nutrient enrichment. J Geophys Res 110:C09S07

    Google Scholar 

  • Laurent J, Tambutté S, Tambutté E, Allemand D, Venn A (2013) The influence of photosynthesis on host intracellular pH in scleractinian corals. J Exp Biol 216:1398–1404

    Article  PubMed  CAS  Google Scholar 

  • Laurent J, Venn A, Tambutté E, Ganot P, Allemand D, Tambutté S (2014) Regulation of intracellular pH in cnidarians: response to acidosis in Anemonia viridis. FEBS J 281:683–695

    Article  PubMed  CAS  Google Scholar 

  • Leal MC, Jesus B, Ezequiel J, Calado R, Rocha RJM, Cartaxana P, Serodio J (2015) Concurrent imaging of chlorophyll fluorescence, Chlorophyll a content and green fluorescent proteins-like proteins of symbiotic cnidarians. Mar Ecol Evol Perspect 36(3):572–584

    Google Scholar 

  • Lesser MP, Mazel CH, Gorbunov MY, Falkowski PG (2014) Discovery of symbiotic nitrogen-fixing cyanobacteria in corals. Science 305:1–5

    Google Scholar 

  • Leutenegger A, D’Angelo C, Matz MV, Denzel A, Oswald F, Salih A, Nienhaus GU, Wiedenmann J (2007) It’s cheap to be colorful. Anthozoans show a slow turnover of GFP-like proteins. FEBS J 274:2496–2505

    Article  PubMed  CAS  Google Scholar 

  • Little AF, van Oppen MJ, Willis BL (2004) Flexibility in algal endosymbioses shapes growth in reef corals. Science 304:1492–1494

    Article  PubMed  CAS  Google Scholar 

  • Lüthi D, Le Floch M, Bereiter B, Blunier T, Barnola J-M, Siegenthaler U, Raynaud D, Jouzel J, Fischer H, Kawamura K et al (2008) High-resolution carbon dioxide concentration record 650,000–800,000 years before present. Nature 453:379–382

    Article  PubMed  CAS  Google Scholar 

  • Marker M, Kline DI, Kirkwood WJ, Headley K, Brewer PG, Peltzer ET, Miard T, Chai A, James M, Schneider K et al (2010) The coral proto free ocean carbon enrichment system (CP-FOCE): engineering and development, Proceedings of OCEANS IEEE 1–10

    Google Scholar 

  • Matz MV, Fradkov AF, Labas YA, Savitsky AP, Zaraisky AG, Markelov ML, Lukyanov SA (1999) Fluorescent proteins from nonbioluminescent Anthozoa species. Nat Biotechnol 17:969–973

    Google Scholar 

  • Marshall AT (1996) Calcification in hermatypic and ahermatypic corals. Science 271:637–639

    Article  CAS  Google Scholar 

  • Mass T, Drake JL, Haramaty L, Kim JD, Zelzion E, Bhattacharya D, Falkowski PG (2013) Cloning and characterization of four novel coral acid-rich proteins that precipitate carbonates in vitro. Curr Biol 23:1126–1131

    Article  PubMed  CAS  Google Scholar 

  • Mass T, Drake JL, Peters EC, Jiang W, Falkowski PG (2014) Immunolocalization of skeletal matrix proteins in tissue and mineral of the coral Stylophora pistillata. Proc Natl Acad Sci U S A 111:12728–12733

    Google Scholar 

  • McLean PF, Cooley L (2013) Protein equilibration through somatic ring canals in Drosophila. Science 340(6139):1445–1447

    Google Scholar 

  • Millero FJ (2007) The marine inorganic carbon cycle. Chem Rev 107:308–341

    Article  PubMed  CAS  Google Scholar 

  • Morita M, Suwa R, Iguchi A, Nakamura M, Shimada K, Sakai K, Suzuki A (2010) Ocean acidification reduces sperm flagellar motility in broadcast spawning reef invertebrates. Zygote 18:103–107

    Article  PubMed  CAS  Google Scholar 

  • Moya A, Tambutté S, Bertucci A, Tambutté E, Lotto S, Vullo D, Supuran CT, Allemand D, Zoccola D (2008) Carbonic anhydrase in the scleractinian coral Stylophora pistillata: characterization, localization, and role in biomineralization. J Biol Chem 283:25475–25484

    Google Scholar 

  • Muscatine L (1973) Nutrition of corals. In: Jones OA, Endean R (eds) Biology and geology of coral reefs, vol II, Biology I. Academic, New York, pp 77–115

    Chapter  Google Scholar 

  • Muscatine L (1990) The role of symbiotic algae in carbon and energy flux in reef corals. In: Dubinsky Z (ed) Ecosystems of the world. Elsevier, Amsterdam, pp 75–87

    Google Scholar 

  • Muscatine L, Cernichiari E (1969) Assimilation of photosynthetic products of zooxanthellae by a reef coral. Biol Bull 137:506–523

    Article  CAS  Google Scholar 

  • Muscatine L, Falkowski PG, Porter JW, Dubinsky Z (1984) Fate of the photosynthetic fixed carbon in light-and shade-adapted colonies of the symbiotic coral Stylophora pistillata. Proc R Soc B Biol Sci 222:181–202

    Article  CAS  Google Scholar 

  • Nakamura M, Ohki S, Suzuki A, Sakai K (2011) Coral larvae under ocean acidification: survival, metabolism, and metamorphosis. PLoS One 6:e14521–e14527

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Odorico DM, Miller DJ (1997) Variation in the ribosomal internal transcribed spacers and 5.8S rDNA among five species of Acropora (Cnidaria; Scleractinia): patterns of variation consistent with reticulate evolution. Mol Biol Evol 14:465–473

    Google Scholar 

  • Ohde S, van Woesik R (1999) Carbon dioxide flux and metabolic processes of a coral reef, Okinawa. Bull Mar Sci 65:559–576

    Google Scholar 

  • Ohmiya Y, Hirano T (1996) Shining the light: the mechanism of the bioluminescence reaction of calcium-binding photoproteins. Chem Biol 3:337–347

    Google Scholar 

  • Oswald F, Schmitt F, Leutenegger A, Ivanchenko S, D’Angelo C, Salih A, Maslakova S, Bulina M, Schirmbeck R, Nienhaus GU, Matz MV, Wiedenmann J (2007) Contributions of host and symbiont pigments to the coloration of reef corals. FEBS J 274(4):1102–1109

    Google Scholar 

  • Pagani M, Liu ZH, LaRiviere J, Ravelo AC (2010) High earth-system climate sensitivity determined from Pliocene carbon dioxide concentrations. Nat Geosci 3:27–30

    Article  CAS  Google Scholar 

  • Palmer CV, Roth MS, Gates RD (2009) Red fluorescent protein responsible for pigmentation in trematode-infected Porites compressa tissues. Biol Bull 216:68–74

    Google Scholar 

  • Petersen OH, Petersen C (1994) Calcium and hormone action. Annu Rev Physiol 56:297–319

    Google Scholar 

  • Phillips JH (1963) Immune mechanisms in the phylum Coelenterata. In: Dougherty EC (ed) The lower metazoa. University of California Press, Berkeley, pp 425–431

    Google Scholar 

  • Price NN, Martz TR, Brainard RE, Smith JE (2012) Diel variability in seawater pH relates to calcification and benthic community structure on coral reefs. PLoS One 7:e43843

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Putnam RW, Roos A (1997) Intracellular pH. In: Hoffman JF, Jamieson DJ (eds) Handbook of physiology. Oxford University Press, New York, pp 389–440

    Google Scholar 

  • Puverel S, Tambutt E, Zoccola D, Domart-Coulon I, Bouchot A, Lotto SV, Allemand D, Tambutt S (2004) Antibodies against the organic matrix in scleractinians: a new tool to study coral biomineralization. Coral Reefs 24:149–156

    Article  Google Scholar 

  • Puverel S, Tambutté E, Pereira-Mouriès L, Zoccola D, Allemand D, Tambutté S (2005) Soluble organic matrix of two Scleractinian corals: partial and comparative analysis. Comp Biochem Physiol B Biochem Mol Biol 141:480–487

    Article  PubMed  CAS  Google Scholar 

  • Raina J-B, Dinsdale EA, Willis BL, Bourne DG (2010) Do the organic sulfur compounds DMSP and DMS drive coral microbial associations? Trends Microbiol 18:101–108

    Article  PubMed  CAS  Google Scholar 

  • Ries JB (2011) A physicochemical framework for interpreting the biological calcification response to CO2-induced ocean acidification. Geochim Cosmochim Acta 75:4053–4064

    Article  CAS  Google Scholar 

  • Rocca JD, Hall EK, Lennon JT, Evans SE, Waldrop MP, Cotner JB, Nemergut DR, Graham EB, Wallenstein MD (2015) Relationships between protein-encoding gene abundance and corresponding process are commonly assumed yet rarely observed. ISME J 9:1693–1699

    Article  PubMed  CAS  Google Scholar 

  • Rohwer F, Seguritan V, Azam F, Knowlton N (2002) Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser 243:1–10

    Article  Google Scholar 

  • Romano SL, Cairns SD (2000) Molecular phylogenetic hypotheses for the evolution of scleractinian corals. Bull Mar Sci 67:1043–1068

    Google Scholar 

  • Romano SL, Palumbi SR (1996) Evolution of scleractinian corals inferred from molecular systematics. Science 271:640–642

    Article  CAS  Google Scholar 

  • Roos A, Boron WF (1981) Intracellular pH. Physiol Rev 61:296–434

    PubMed  CAS  Google Scholar 

  • Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I (2007) The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol 5:355–362

    Article  PubMed  CAS  Google Scholar 

  • Roth MS (2014) The engine of the reef: photobiology of the coral-algal symbiosis. Front Microbiol 5:422

    Article  PubMed  PubMed Central  Google Scholar 

  • Roth MS, Deheyn DD (2013) Effects of cold stress and heat stress on coral fluorescence in reef-building corals. Sci Rep 3:1421

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Roth MS, Fan T-Y, Deheyn DD (2013) Life history changes in coral fluorescence and the effects of light intensity on larval physiology and settlement in Seriatopora hystrix. PLoS One 8:e59476

    Article  PubMed  PubMed Central  Google Scholar 

  • Roth MS, Goericke R, Deheyn DD (2012) Cold induces acute stress but heat is ultimately more deleterious for the reef-building coral Acropora yongei. Sci Rep 2:240

    Google Scholar 

  • Roth MS, Latz MI, Goericke R, Deheyn DD (2010) Green fluorescent protein regulation in the coral Acropora yongei during photoacclimation. J Exp Biol 213:3644–3655

    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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sabine CL, Feely RA, Gruber N, Key RM, Lee K, Bullister JL, Wanninkhof R, Wong CS, Wallace DW, Tilbrook B et al (2004) The oceanic sink for anthropogenic CO2. Science 305:367–371

    Article  PubMed  CAS  Google Scholar 

  • Salih A, Larkum A, Cox G, Kühl M, Hoegh-Guldberg O (2000) Fluorescent pigments in corals are photoprotective. Nature 408:850–853

    Article  PubMed  CAS  Google Scholar 

  • Schlichter D, Meier U, Fricke HW (1994) Improvement of photosynthesis in zooxanthellate corals by autofluorescent chromatophores. Oecologia 99:124–131

    Article  Google Scholar 

  • Schonknecht G, Brown JE, Verchot-Lubicz J (2008) Plasmodesmata transport of GFP alone or fused to potato virus X TGBp1 is diffusion driven. Protoplasma 232(3–4):143–152

    Google Scholar 

  • Schweinsberg M, Weiss LC, Striewski S, Tollrian R, Lampert KP (2015) More than one genotype: how common is intracolonial genetic variability in scleractinian corals? Mol Ecol 24:2673–2685

    Article  PubMed  Google Scholar 

  • Shashar N, Cohen Y, Loya Y (1993) Extreme diel fluctuations of oxygen in diffusive boundary layers surrounding stony corals. Biol Bull 185:455–461

    Article  Google Scholar 

  • Shaw EC, Mcneil BI, Tibrook B (2012) Impacts of ocean acidification in naturally variable coral reef flat ecosystems. J Geophys Res Oceans 117:C03038

    Article  CAS  Google Scholar 

  • Shinomura O, Johnson FH, Saiga Y (1962) Extraction, purification and properties of aequorin, a bioluminescent protein from the luminous hydromedusan, Aequorea. J Cell Comp Physiol 59:223–239

    Article  Google Scholar 

  • Shinzato C, Shoguchi E, Kawashima T, Hamada M, Hisata K, Tanaka M, Fujie M, Fujiwara M, Koyanagi R, Ikuta T et al (2011) Using the Acropora digitifera genome to understand coral responses to environmental change. Nature 476:320–323

    Google Scholar 

  • Silverman J, Kline DI, Johnson L, Rivlin T, Schneider K, Erez J, Lazar B, Caldeira K (2012) Carbon turnover rates in the one tree Island reef: a 40-year perspective. Geophys Res Biogeosci 1127:G03023

    Google Scholar 

  • Silverman J, Lazar B, Cao L, Caldeira K, Erez J (2009) Coral reefs may start dissolving when atmospheric CO2 doubles. Geophys Res Lett 36:L05606

    Article  CAS  Google Scholar 

  • Smith EG, Angelo D, Salih C, Wiedenmann J (2013) Screening by coral green fluorescent protein (GFP)-like chromoproteins supports a role in photoprotection of zooxanthellae. Coral Reefs 32:463–474

    Article  Google Scholar 

  • Stolarski J, Kitahara MV, Miller DJ, Cairns SD, Mazur M, Meibom A (2011) The ancient evolutionary origins of Scleractinia revealed by azooxanthellate corals. BMC Evol Biol 11:316

    Article  PubMed  PubMed Central  Google Scholar 

  • Tambutté E, Allemand D, Mueller E, Jaubert J (1996) A compartmental approach to the mechanism of calcification in hermatypic corals. J Exp Biol 199:1029–1041

    Google Scholar 

  • Tambutté E, Tambutté S, Segonds N, Zoccola D, Venn A, Erez J, Allemand D (2011) Calcein labelling and electrophysiology: insights on coral tissue permeability and calcification. Proc R Soc B BiolSci 279:19–27

    Article  CAS  Google Scholar 

  • Tresguerres M (2014) sAC from aquatic organisms as a model to study the evolution of acid/base sensing. BBA Mol Basis Dis 1842:2629–2635

    Article  CAS  Google Scholar 

  • Tresguerres M, Barott KL, Barron ME, Roa JN (2014) Established and potential physiological roles of bicarbonate-sensing soluble adenylyl cyclase (sAC) in aquatic animals. J Exp Biol 217:663–672

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tresguerres M, Buck J, Levin LR (2010a) Physiological carbon dioxide, bicarbonate, and pH sensing. Pflugers Arch Eur J Physiol 460:953–964

    Article  CAS  Google Scholar 

  • Tresguerres M, Levin LR, Buck J (2011) Intracellular cAMP signaling by soluble adenylyl cyclase. Kidney Int 79:1277–1288

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tresguerres M, Parks SK, Katoh F, Goss GG (2006) Microtubule-dependent relocation of branchial V-H+−ATPase to the basolateral membrane in the Pacific spiny dogfish (Squalus acanthias): a role in base secretion. J Exp Biol 209:599–609

    Google Scholar 

  • Tresguerres M, Parks SK, Salazar E, Levin LR, Goss GG, Buck J (2010b) Bicarbonate-sensing soluble adenylyl cyclase is an essential sensor for acid/base homeostasis. Proc Natl Acad Sci U S A 107:442–447

    Article  PubMed  CAS  Google Scholar 

  • van Oppen MJ, McDonald BJ, Willis B, Miller DJ (2001) The evolutionary history of the coral genus Acropora (Scleractinia, Cnidaria) based on a mitochondrial and a nuclear marker: reticulation, incomplete lineage sorting, or morphological convergence? Mol Biol Evol 18:1315–1329

    Google Scholar 

  • Vandermeulen JH, Watabe N (1973) Studies on reef corals. I. Skeleton formation by newly settled planula larva of Pocillopora damicornis. Mar Biol 23:47–57

    Google Scholar 

  • Venn AA, Tambutté E, Lotto S, Zoccola D, Allemand D, Tambutté S (2009) Imaging intracellular pH in a reef coral and symbiotic anemone. Proc Natl Acad Sci U S A 106:16574–16579

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Venn A, Tambutté E, Holcomb M, Allemand D, Tambutté S (2011) Live tissue imaging shows reef corals elevate pH under their calcifying tissue relative to seawater. PLoS One 6:e20013–e20019

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Veron JE (1993) Corals of Australia and the Indo-Pacific, 2nd edn. University of Hawaii Press, Honolulu

    Google Scholar 

  • Vidal-Dupiol J, Zoccola D, Tambutté E, Grunau C, Cosseau C, Smith KM, Freitag M, Dheilly NM, Allemand D, Tambutté S (2013) Genes related to Ion-transport and energy production are upregulated in response to CO2-driven pH decrease in corals: new insights from transcriptome analysis. PLoS One 8:e58652

    Google Scholar 

  • Wainwright SA (1964) Studies of the mineral phase of coral skeleton. Exp Cell Res 34:213–230

    Article  CAS  Google Scholar 

  • Weis VM, Smith GJ, Muscatine L (1989) A “CO2 supply” mechanism in zooxanthellate cnidarians: role of carbonic anhydrase. Mar Biol 100:195–202

    Article  CAS  Google Scholar 

  • Wiedenmann J, Ivanchenko S, Oswald F, Nienhaus GU (2004) Identification of GFP-like proteins in nonbioluminescent, azooxanthellate anthozoa opens new perspectives for bioprospecting. Marine Biotechnol 6(3):270–277

    Google Scholar 

  • Wijgerde T, Jurriaans S, Hoofd M, Verreth JA, Osinga R (2012) Oxygen and heterotrophy affect calcification of the scleractinian coral Galaxea fascicularis. PLoS One 7:e52702

    Google Scholar 

  • Wijgerde T, Silva CIF, Scherders V, van Bleijswijk J, Osinga R (2014) Coral calcification under daily oxygen saturation and pH dynamics reveals the important role of oxygen. Biol Open 3:489–493

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wijsman-Best M (1975) Intra-and extratentacular budding in hermatypic reef corals. pp. 471–475

    Google Scholar 

  • Wild C, Huettel M, Klueter A, Kremb SG, Rasheed MY, Jørgensen BB (2004) Coral mucus functions as an energy carrier and particle trap in the reef ecosystem. Nature 428:66–70

    Article  PubMed  CAS  Google Scholar 

  • Willis BL, Babcock RC, Harrison PL, Wallace CC (1997) Experimental hybridization and breeding incompatibilities with the mating systems of mass spawning reef corals. Coral Reefs 16:S53–S65

    Article  Google Scholar 

  • Wong W, Scott JD (2004) AKAP signalling complexes: focal points in space and time. Nat Rev Mol Cell Biol 5:959–970

    Google Scholar 

  • Yates KK, Halley RB (2003) Measuring coral reef community metabolism using new benthic chamber technology. Coral Reefs 22:247–255

    Article  Google Scholar 

  • Yates KK, Halley RB (2006) Diurnal variation in rates of calcification and carbonate sediment dissolution in Florida Bay. Estuar Coast 29:24–39

    Article  CAS  Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zoccola D, Tambutté E, Kulhanek E, Puverel S, Scimeca J-C, Allemand D, Tambutté S (2004) Molecular cloning and localization of a PMCA P-type calcium ATPase from the coral Stylophora pistillata. Biochim Biophys Acta 1663:117–126

    Google Scholar 

  • Zoccola D, Tambutté E, Sénégas-Balas F, Michelis J-F, Failla J-P, Jaubert J, Allemand D (1999) Cloning of a calcium channel a1 subunit from the reef-building coral, Stylophora pistillata. Gene 227:157–167

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Supported by NSF grant #1220641 (MT and DDD), NSF grant#1538495 (DIK and MT), and Alfred P. Sloan Research Fellowship #BR2013-103 (MT). Special thanks to Mr. Garfield Kwan for his help with . Fig. 7.1b.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Martin Tresguerres .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Tresguerres, M., Barott, K.L., Barron, M.E., Deheyn, D.D., Kline, D.I., Linsmayer, L.B. (2017). Cell Biology of Reef-Building Corals: Ion Transport, Acid/Base Regulation, and Energy Metabolism. In: Weihrauch, D., O’Donnell, M. (eds) Acid-Base Balance and Nitrogen Excretion in Invertebrates. Springer, Cham. https://doi.org/10.1007/978-3-319-39617-0_7

Download citation

Publish with us

Policies and ethics