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

  • Martin TresguerresEmail author
  • Katie L. Barott
  • Megan E. Barron
  • Dimitri D. Deheyn
  • David I. Kline
  • Lauren B. Linsmayer


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.


Bleaching Calcification Carbon-concentrating mechanism Fluorescent protein Na+/K+-ATPase Ocean acidification Photosynthesis pH Vacuolar H+-ATPase 



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.


  1. 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 31:147–156CrossRefGoogle Scholar
  2. 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 288:1–15CrossRefGoogle Scholar
  3. 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 107:20400–20404Google Scholar
  4. 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
  5. Allemand D, Furla P, Bénazet-Tambutté S (1998) Mechanisms of carbon acquisition for endosymbiont photosynthesis in Anthozoa. Can J Bot 76:925–941Google Scholar
  6. 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 3:453–467Google Scholar
  7. 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 119–150CrossRefGoogle Scholar
  8. 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 5:5741PubMedCrossRefGoogle Scholar
  9. Andersson AJ, Gledhill D (2013) Ocean acidification and coral reefs: effects on breakdown, dissolution, and net ecosystem calcification. Ann Rev Mar Sci 5:321–348PubMedCrossRefGoogle Scholar
  10. 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 28:16–27CrossRefGoogle Scholar
  11. 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 105:17442–17446PubMedPubMedCentralCrossRefGoogle Scholar
  12. Babcock RC, Heyward AJ (1986) Larval development of certain gamete-spawning scleractinian corals. Coral Reefs 5:111–116CrossRefGoogle Scholar
  13. 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 3:1–7CrossRefGoogle Scholar
  14. 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–R246PubMedCrossRefGoogle Scholar
  15. 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 112:607–612PubMedCrossRefGoogle Scholar
  16. 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 7:2509–2530CrossRefGoogle Scholar
  17. Beerling DJ, Royer DL (2011) Convergent Cenozoic CO2 history. Nat Geosci 4:418–420CrossRefGoogle Scholar
  18. Ben-Zvi O, Eyal G, Loya Y (2015) Light-dependent fluorescence in the coral Galaxea fascicularis. Hydrobiologia 759:15–26CrossRefGoogle Scholar
  19. Benson AA, Patton JS, Abraham S (1978) Energy exchange in coral reef ecosystems. Atoll Res Bull 220:33–54CrossRefGoogle Scholar
  20. 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 277:87–95Google Scholar
  21. 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 YorkGoogle Scholar
  22. 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 9:1–11Google Scholar
  23. Bou-Abdallah F, Chasteen ND, Lesser MP (2006) Quenching of superoxide radicals by green fluorescent protein. Biochim Biophys Acta Gen Subj 1760(11):1690–1695Google Scholar
  24. Bourne GC (1900) The anthozoa. In: Lankester ER (ed) A treatise on zoology. Part II. The porifera and coelenterata. Adam & Charles Black, London, pp 1–84Google Scholar
  25. 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 96:79–84Google Scholar
  26. Burke L, Reytar K, Spalding M, Perry A (2011) Reefs at risk revisited. World Resources Institute, Washington, DCGoogle Scholar
  27. Burriesci MS, Raab TK, Pringle JR (2012) Evidence that glucose is the major transferred metabolite in dinoflagellate-cnidarian symbiosis. J Exp Biol 215:3467–3477PubMedPubMedCentralCrossRefGoogle Scholar
  28. Caldeira K, Wickett ME (2003) Oceanography: anthropogenic carbon and ocean pH. Nature 425:365PubMedCrossRefGoogle Scholar
  29. 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 281:20141856Google Scholar
  30. Catala-Stucki R (1959) Fluorescent effects from corals irradiated with ultra-violet rays. Nature 183:949CrossRefGoogle Scholar
  31. 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 190:323–331CrossRefGoogle Scholar
  32. 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 289:625–628Google Scholar
  33. 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 31:312–319PubMedCrossRefGoogle Scholar
  34. Clode PL, Marshall AT (2002) Low temperature FESEM of the calcifying interface of a scleractinian coral. Tissue Cell 34:187–198PubMedCrossRefGoogle Scholar
  35. Cohen A, Holcomb M (2009) Why corals care about ocean acidification. Oceanography 22:118–127CrossRefGoogle Scholar
  36. Cohen AL, McConnaughey TA (2003) Geochemical perspectives on coral mineralization. Rev Mineral Geochem 54:151–187Google Scholar
  37. Crossland CJ, Barnes DJ, Borowitzka MA (1980) Diurnal lipid and mucus production in the staghorn coral Acropora acuminata. Mar Biol 60:81–90CrossRefGoogle Scholar
  38. 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 282:20141725PubMedPubMedCentralCrossRefGoogle Scholar
  39. 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 96:1411–1420PubMedCrossRefGoogle Scholar
  40. Davies PS (1984) The role of zooxanthellae in the nutritional energy requirements of Pocillopora eydouxi. Coral Reefs 2:181–186Google Scholar
  41. Davy SK, Allemand D, Weis VM (2012) Cell biology of cnidarian-dinoflagellate symbiosis. Microbiol Mol Biol Rev 76:229–261PubMedPubMedCentralCrossRefGoogle Scholar
  42. Dawson TL (2007) Light-harvesting and light-protecting pigments in simple life forms. Color Technol 123:129–142CrossRefGoogle Scholar
  43. 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 139:221–233CrossRefGoogle Scholar
  44. 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):288–297Google Scholar
  45. 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):197–204Google Scholar
  46. 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 3:1523–1533CrossRefGoogle Scholar
  47. 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 111:12728–12733PubMedPubMedCentralCrossRefGoogle Scholar
  48. Ducklow HW, Mitchell R (1979) Composition of mucus released by coral reef coelenterates. Limnol Oceanogr 24:706–714CrossRefGoogle Scholar
  49. 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 279:2951–2958PubMedPubMedCentralCrossRefGoogle Scholar
  50. Erez J (1978) Vital effect on stable-isotope composition seen in foraminifera and coral skeletons. Nature 273:199–202CrossRefGoogle Scholar
  51. 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 1:165–169CrossRefGoogle Scholar
  52. Falkowski PG, Dubinsky Z, Muscatine L, Porter JW (1984) Light and bioenergetics of a symbiotic coral. BioScience 34:705–709CrossRefGoogle Scholar
  53. 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:e3251PubMedPubMedCentralCrossRefGoogle Scholar
  54. 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 305:362–366PubMedCrossRefGoogle Scholar
  55. Friedman PA, Gesek FA (1995) Cellular calcium transport in renal epithelia: measurement, mechanisms, and regulation. Physiol Rev 75:429–471Google Scholar
  56. 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 427:832–835PubMedCrossRefGoogle Scholar
  57. 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 274:303–310Google Scholar
  58. Furla P, Galgani I, Durand I, Allemand D (2000) Sources and mechanisms of inorganic carbon transport for coral calcification and photosynthesis. J Exp Biol 203:3445–3457PubMedGoogle Scholar
  59. 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 SpringGoogle Scholar
  60. 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 32:44–62PubMedCrossRefGoogle Scholar
  61. 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 39:160–183CrossRefGoogle Scholar
  62. Gattuso JP, Hendriks IE, Brewer PG (2014) Free-ocean CO2 enrichment (FOCE) systems: present status and future developments. Biogeosciences 11:4057–4075CrossRefGoogle Scholar
  63. 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–C1316Google Scholar
  64. 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 217:1963–1969PubMedCrossRefGoogle Scholar
  65. Gladfelter EH (1983) Circulation of fluids in the gastrovascular system of the reef coral Acropora cervicornis. Biol Bull 165:619–636CrossRefGoogle Scholar
  66. Goldberg WM (2001a) Acid polysaccharides in the skeletal matrix and calicoblastic epithelium of the stony coral Mycetophyllia reesi. Tissue Cell 33:376–387PubMedCrossRefGoogle Scholar
  67. Goldberg WM (2001b) Desmocytes in the calicoblastic epithelium of the stony coral Mycetophyllia reesi and their attachment to the skeleton. Tissue Cell 33:388–394PubMedCrossRefGoogle Scholar
  68. Goldberg WM (2002a) Feeding behavior, epidermal structure and mucus cytochemistry of the scleractinian Mycetophyllia reesi, a coral without tentacles. Tissue Cell 34:232–245PubMedCrossRefGoogle Scholar
  69. Goldberg WM (2002b) Gastrodermal structure and feeding responses in the scleractinian Mycetophyllia reesi, a coral with novel digestive filaments. Tissue Cell 34:246–261PubMedCrossRefGoogle Scholar
  70. 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 116:59–75CrossRefGoogle Scholar
  71. 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 117:239–250CrossRefGoogle Scholar
  72. Goreau TF, Goreau NI, Yonge CM (1971) Reef corals: autotrophs or heterotrophs? Biol Bull 141:247–260CrossRefGoogle Scholar
  73. 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 PubMedPubMedCentralCrossRefGoogle Scholar
  74. Haddock SHD, Moline MA, Case JF (2009) Bioluminescence in the sea. 2:443–493.
  75. 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 454:96–99PubMedCrossRefGoogle Scholar
  76. Hanson MR, Kohler RH (2001) GFP imaging: methodology and application to investigate cellular compartmentation in plants. J Exp Bot 52(356):529–539Google Scholar
  77. 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 9:249–259PubMedPubMedCentralCrossRefGoogle Scholar
  78. Hosey MM, Lazdunski M (1988) Calcium channels: molecular pharmacology, structure and regulation. J Membr Biol 104:81–105PubMedCrossRefGoogle Scholar
  79. Hughes AD, Grottoli AG, Pease TK, Matsui Y (2010) Acquisition and assimilation of carbon in non-bleached and bleached corals. Mar Ecol Prog Ser 420:91–101CrossRefGoogle Scholar
  80. Ip YK, Lim ALL, Lim RW (1991) Some properties of calcium activated adenosine triphosphatase from the hermatypic coral Galaxea fascicularis. Mar Biol 111:191–197CrossRefGoogle Scholar
  81. Isa Y (1986) An electron microscope study on the mineralization of the skeleton of the staghorn coral Acropora hebes. Mar Biol 93:91–101CrossRefGoogle Scholar
  82. Johnston IS (1980) The ultrastructure of skeletogenesis in hermatypic corals. Int Rev Cytol 67:171–214CrossRefGoogle Scholar
  83. 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 409:1–12CrossRefGoogle Scholar
  84. Jokiel PL (2011b) Ocean acidification and control of reef coral calcification by boundary layer limitation of proton flux. Bull Mar Sci 87:639–657CrossRefGoogle Scholar
  85. Jokiel PL (2013) Coral reef calcification: carbonate, bicarbonate and proton flux under conditions of increasing ocean acidification. Proc Biol Sci 280:20130031PubMedPubMedCentralCrossRefGoogle Scholar
  86. 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:e34659PubMedPubMedCentralCrossRefGoogle Scholar
  87. 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:e88615Google Scholar
  88. 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 2:199–208Google Scholar
  89. Kawaguti S (1969) The effect of green fluorescent pigment on the productivity of the reef corals. Micronesica 5:313Google Scholar
  90. Kawaguti S, Sakumoto D (1948) The effect of light on the calcium deposition of corals. Bul Oceanogr Inst Taiwan 4:65–70Google Scholar
  91. 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):1125–1133Google Scholar
  92. 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 278:2691–2697PubMedPubMedCentralCrossRefGoogle Scholar
  93. 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, DCGoogle Scholar
  94. 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:e0127648PubMedPubMedCentralCrossRefGoogle Scholar
  95. 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 2:413PubMedPubMedCentralCrossRefGoogle Scholar
  96. 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 280:20122328PubMedPubMedCentralCrossRefGoogle Scholar
  97. Kroeker KJ, Kordas RL, Crim RN, Singh GG (2010) Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecol Lett 13:1419–1434PubMedCrossRefGoogle Scholar
  98. Kroeker KJ, Micheli F, Gambi MC (2013) Ocean acidification causes ecosystem shifts via altered competitive interactions. Nat Clim Chang 3:156–159CrossRefGoogle Scholar
  99. 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 117:159–172Google Scholar
  100. 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):4256–4261Google Scholar
  101. 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:C09S07Google Scholar
  102. 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 216:1398–1404PubMedCrossRefGoogle Scholar
  103. 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 281:683–695PubMedCrossRefGoogle Scholar
  104. 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):572–584Google Scholar
  105. Lesser MP, Mazel CH, Gorbunov MY, Falkowski PG (2014) Discovery of symbiotic nitrogen-fixing cyanobacteria in corals. Science 305:1–5Google Scholar
  106. 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 274:2496–2505PubMedCrossRefGoogle Scholar
  107. Little AF, van Oppen MJ, Willis BL (2004) Flexibility in algal endosymbioses shapes growth in reef corals. Science 304:1492–1494PubMedCrossRefGoogle Scholar
  108. 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 453:379–382PubMedCrossRefGoogle Scholar
  109. 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 1–10Google Scholar
  110. Matz MV, Fradkov AF, Labas YA, Savitsky AP, Zaraisky AG, Markelov ML, Lukyanov SA (1999) Fluorescent proteins from nonbioluminescent Anthozoa species. Nat Biotechnol 17:969–973Google Scholar
  111. Marshall AT (1996) Calcification in hermatypic and ahermatypic corals. Science 271:637–639CrossRefGoogle Scholar
  112. 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 23:1126–1131PubMedCrossRefGoogle Scholar
  113. 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 111:12728–12733Google Scholar
  114. McLean PF, Cooley L (2013) Protein equilibration through somatic ring canals in Drosophila. Science 340(6139):1445–1447Google Scholar
  115. Millero FJ (2007) The marine inorganic carbon cycle. Chem Rev 107:308–341PubMedCrossRefGoogle Scholar
  116. 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 18:103–107PubMedCrossRefGoogle Scholar
  117. 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 283:25475–25484Google Scholar
  118. 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 77–115CrossRefGoogle Scholar
  119. 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 75–87Google Scholar
  120. Muscatine L, Cernichiari E (1969) Assimilation of photosynthetic products of zooxanthellae by a reef coral. Biol Bull 137:506–523CrossRefGoogle Scholar
  121. 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 222:181–202CrossRefGoogle Scholar
  122. Nakamura M, Ohki S, Suzuki A, Sakai K (2011) Coral larvae under ocean acidification: survival, metabolism, and metamorphosis. PLoS One 6:e14521–e14527PubMedPubMedCentralCrossRefGoogle Scholar
  123. 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 14:465–473Google Scholar
  124. Ohde S, van Woesik R (1999) Carbon dioxide flux and metabolic processes of a coral reef, Okinawa. Bull Mar Sci 65:559–576Google Scholar
  125. Ohmiya Y, Hirano T (1996) Shining the light: the mechanism of the bioluminescence reaction of calcium-binding photoproteins. Chem Biol 3:337–347Google Scholar
  126. 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):1102–1109Google Scholar
  127. Pagani M, Liu ZH, LaRiviere J, Ravelo AC (2010) High earth-system climate sensitivity determined from Pliocene carbon dioxide concentrations. Nat Geosci 3:27–30CrossRefGoogle Scholar
  128. Palmer CV, Roth MS, Gates RD (2009) Red fluorescent protein responsible for pigmentation in trematode-infected Porites compressa tissues. Biol Bull 216:68–74Google Scholar
  129. Petersen OH, Petersen C (1994) Calcium and hormone action. Annu Rev Physiol 56:297–319Google Scholar
  130. Phillips JH (1963) Immune mechanisms in the phylum Coelenterata. In: Dougherty EC (ed) The lower metazoa. University of California Press, Berkeley, pp 425–431Google Scholar
  131. 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:e43843PubMedPubMedCentralCrossRefGoogle Scholar
  132. Putnam RW, Roos A (1997) Intracellular pH. In: Hoffman JF, Jamieson DJ (eds) Handbook of physiology. Oxford University Press, New York, pp 389–440Google Scholar
  133. 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 24:149–156CrossRefGoogle Scholar
  134. 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 141:480–487PubMedCrossRefGoogle Scholar
  135. Raina J-B, Dinsdale EA, Willis BL, Bourne DG (2010) Do the organic sulfur compounds DMSP and DMS drive coral microbial associations? Trends Microbiol 18:101–108PubMedCrossRefGoogle Scholar
  136. Ries JB (2011) A physicochemical framework for interpreting the biological calcification response to CO2-induced ocean acidification. Geochim Cosmochim Acta 75:4053–4064CrossRefGoogle Scholar
  137. 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 9:1693–1699PubMedCrossRefGoogle Scholar
  138. Rohwer F, Seguritan V, Azam F, Knowlton N (2002) Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser 243:1–10CrossRefGoogle Scholar
  139. Romano SL, Cairns SD (2000) Molecular phylogenetic hypotheses for the evolution of scleractinian corals. Bull Mar Sci 67:1043–1068Google Scholar
  140. Romano SL, Palumbi SR (1996) Evolution of scleractinian corals inferred from molecular systematics. Science 271:640–642CrossRefGoogle Scholar
  141. Roos A, Boron WF (1981) Intracellular pH. Physiol Rev 61:296–434PubMedGoogle Scholar
  142. 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 5:355–362PubMedCrossRefGoogle Scholar
  143. Roth MS (2014) The engine of the reef: photobiology of the coral-algal symbiosis. Front Microbiol 5:422PubMedPubMedCentralCrossRefGoogle Scholar
  144. Roth MS, Deheyn DD (2013) Effects of cold stress and heat stress on coral fluorescence in reef-building corals. Sci Rep 3:1421PubMedPubMedCentralCrossRefGoogle Scholar
  145. 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:e59476PubMedPubMedCentralCrossRefGoogle Scholar
  146. 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 2:240Google Scholar
  147. Roth MS, Latz MI, Goericke R, Deheyn DD (2010) Green fluorescent protein regulation in the coral Acropora yongei during photoacclimation. J Exp Biol 213:3644–3655Google Scholar
  148. 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 8:539–553PubMedPubMedCentralCrossRefGoogle Scholar
  149. 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 305:367–371PubMedCrossRefGoogle Scholar
  150. Salih A, Larkum A, Cox G, Kühl M, Hoegh-Guldberg O (2000) Fluorescent pigments in corals are photoprotective. Nature 408:850–853PubMedCrossRefGoogle Scholar
  151. Schlichter D, Meier U, Fricke HW (1994) Improvement of photosynthesis in zooxanthellate corals by autofluorescent chromatophores. Oecologia 99:124–131CrossRefGoogle Scholar
  152. 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):143–152Google Scholar
  153. 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 24:2673–2685PubMedCrossRefGoogle Scholar
  154. Shashar N, Cohen Y, Loya Y (1993) Extreme diel fluctuations of oxygen in diffusive boundary layers surrounding stony corals. Biol Bull 185:455–461CrossRefGoogle Scholar
  155. Shaw EC, Mcneil BI, Tibrook B (2012) Impacts of ocean acidification in naturally variable coral reef flat ecosystems. J Geophys Res Oceans 117:C03038CrossRefGoogle Scholar
  156. 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 59:223–239CrossRefGoogle Scholar
  157. 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 476:320–323Google Scholar
  158. 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:G03023Google Scholar
  159. Silverman J, Lazar B, Cao L, Caldeira K, Erez J (2009) Coral reefs may start dissolving when atmospheric CO2 doubles. Geophys Res Lett 36:L05606CrossRefGoogle Scholar
  160. 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 32:463–474CrossRefGoogle Scholar
  161. 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 11:316PubMedPubMedCentralCrossRefGoogle Scholar
  162. Tambutté E, Allemand D, Mueller E, Jaubert J (1996) A compartmental approach to the mechanism of calcification in hermatypic corals. J Exp Biol 199:1029–1041Google Scholar
  163. 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 279:19–27CrossRefGoogle Scholar
  164. Tresguerres M (2014) sAC from aquatic organisms as a model to study the evolution of acid/base sensing. BBA Mol Basis Dis 1842:2629–2635CrossRefGoogle Scholar
  165. 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 217:663–672PubMedPubMedCentralCrossRefGoogle Scholar
  166. Tresguerres M, Buck J, Levin LR (2010a) Physiological carbon dioxide, bicarbonate, and pH sensing. Pflugers Arch Eur J Physiol 460:953–964CrossRefGoogle Scholar
  167. Tresguerres M, Levin LR, Buck J (2011) Intracellular cAMP signaling by soluble adenylyl cyclase. Kidney Int 79:1277–1288PubMedPubMedCentralCrossRefGoogle Scholar
  168. 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 209:599–609Google Scholar
  169. 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 107:442–447PubMedCrossRefGoogle Scholar
  170. 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 18:1315–1329Google Scholar
  171. Vandermeulen JH, Watabe N (1973) Studies on reef corals. I. Skeleton formation by newly settled planula larva of Pocillopora damicornis. Mar Biol 23:47–57Google Scholar
  172. 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 106:16574–16579PubMedPubMedCentralCrossRefGoogle Scholar
  173. 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–e20019PubMedPubMedCentralCrossRefGoogle Scholar
  174. Veron JE (1993) Corals of Australia and the Indo-Pacific, 2nd edn. University of Hawaii Press, HonoluluGoogle Scholar
  175. 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:e58652Google Scholar
  176. Wainwright SA (1964) Studies of the mineral phase of coral skeleton. Exp Cell Res 34:213–230CrossRefGoogle Scholar
  177. Weis VM, Smith GJ, Muscatine L (1989) A “CO2 supply” mechanism in zooxanthellate cnidarians: role of carbonic anhydrase. Mar Biol 100:195–202CrossRefGoogle Scholar
  178. 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):270–277Google Scholar
  179. 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:e52702Google Scholar
  180. 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 3:489–493PubMedPubMedCentralCrossRefGoogle Scholar
  181. Wijsman-Best M (1975) Intra-and extratentacular budding in hermatypic reef corals. pp. 471–475Google Scholar
  182. 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 428:66–70PubMedCrossRefGoogle Scholar
  183. 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–S65CrossRefGoogle Scholar
  184. Wong W, Scott JD (2004) AKAP signalling complexes: focal points in space and time. Nat Rev Mol Cell Biol 5:959–970Google Scholar
  185. Yates KK, Halley RB (2003) Measuring coral reef community metabolism using new benthic chamber technology. Coral Reefs 22:247–255CrossRefGoogle Scholar
  186. Yates KK, Halley RB (2006) Diurnal variation in rates of calcification and carbonate sediment dissolution in Florida Bay. Estuar Coast 29:24–39CrossRefGoogle Scholar
  187. 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 5:9983PubMedPubMedCentralCrossRefGoogle Scholar
  188. 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 1663:117–126Google Scholar
  189. 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 227:157–167PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2017

Authors and Affiliations

  • Martin Tresguerres
    • 1
    Email author
  • Katie L. Barott
    • 1
  • Megan E. Barron
    • 1
  • Dimitri D. Deheyn
    • 1
  • David I. Kline
    • 1
    • 2
  • Lauren B. Linsmayer
    • 1
  1. 1.Scripps Institution of OceanographyUniversity of California San DiegoLa JollaUSA
  2. 2.Smithsonian Tropical Research InstituteBocas TownPanama

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