Singular physiological behavior of the scleractinian coral Porites astreoides in the dark phase

Abstract

Unlike most other corals that have been declining since the 1980s, the population of Porites astreoides, one of the dominant species of coral in Caribbean reefs, appears to be resilient. We investigated the physiological regulation of the electron transport chain of Symbiodiniaceae chloroplasts during the light/dark transition in P. astreoides compared to nine other common scleractinian corals. Protocols were applied to coral samples in seawater tanks and in situ. The maximum quantum yield (Fv/Fm) in the dark and the effective photochemical efficiency (Fq′/Fm′) in the light were measured during light–dark transitions, and alternative electron flow mechanisms were evaluated using fluorescence variation in response to serial irradiation pulses (SIP protocol). The variation in Fv/Fm (ΔYIImax) was calculated after 3 min or 2 h of dark acclimation (ΔYIImax(2 h); ΔYIImax(3 min)). The three species that belong to the genus Porites (P. astreoides, P. divaricata, P. furcata) showed plastoquinone reduction (PQ) in response to the SIP protocol, unlike all the other species tested. A marked decrease in Fv/Fm (ΔYIImax(2 h) = 47.79%) was observed in P. astreoides in the dark whereas the average ΔYIImax(2 h) of the other species tested was 0.677%. The decrease in ΔYIImax in P. astreoides was due to a significant increase in FoFo(2 h) = − 108.64% ± SD 21.48) whereas Fm remained relatively stable. The increase in Fo was attributed to reduction of the PQ pool through a chlororespiration-like mechanism known to reduce the production of reactive oxygen species. This mechanism was triggered immediately after exposure to the dark, while a brief and moderate light exposure reversed it. Given the ecological success of P. astreoides, we suggest that the high antioxidant capability of this species in the dark phase could be one of the factors favoring its survival in the face of various environmental and anthropogenic threats.

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References

  1. Aihara Y, Takahashi S, Minagawa J (2016) Heat Induction of Cyclic Electron Flow around Photosystem I in the Symbiotic Dinoflagellate Symbiodinium. Plant Physiol 171:522–529

    CAS  PubMed  PubMed Central  Google Scholar 

  2. Alvarez-Filip L, Dulvy NK, Gill JA, Cote IM, Watkinson AR (2009) Flattening of Caribbean coral reefs: region-wide declines in architectural complexity. Proc Biol Sci 276:3019–3025

    PubMed  PubMed Central  Google Scholar 

  3. Beardall J, Quigg A, Raven JA (2003) Oxygen consumption: Photorespiration and chlororespiration. In: Larkum AWD, Douglas SE, Raven JA (eds) Photosynthesis in Algae, vol 14. Springer, Dordrecht, pp 157–181

    Google Scholar 

  4. Bennoun P (1994) Chlororespiration revisited - mitochondrial-plastid interactions in Chlamydomonas. Biochim Biophys Acta 1186:59–66

    CAS  Google Scholar 

  5. Bouchon C, Miller A, Bouchon-Navaro Y, Portillo P, Louis M (2004) Status of coral reefs in the French Caribbean islands and other islands of the Eastern Antilles. In: Wilkinson C (ed) Status of the coral reefs of the world. Australian institue of marine sciences, Australia, pp 493–507

    Google Scholar 

  6. Bouchon C, Portillo P, Bouchon-Navaro Y, Max L, Hoetjes P, Brathwaite A, Roach R, Oxenford H, O’farrell S, Day O (2008a) Status of coral reefs of the Lesser Antilles after the 2005 coral bleaching event. In: Wilkinson C, Souter D (eds) Status of Caribbean coral reefs after bleaching and hurricanes in 2005. Global coral reef monitoring network, and reef and rainforest research centre, Australia, pp 85–103

  7. Bouchon C, Portillo P, Bouchon-Navaro Y, Louis M, Hoetjes P, De Meyer K, Armstrong H, Datadin V, Harding S, Mallela J, Parkinson R, Van Bochove J, Wynne S, Macrae D, Lirman D, Herlan J, Baker A, Collado L, Nimrod S, Mitchell J, Morrall C, Isaac C (2008b) Status of the coral reefs of the Lesser Antilles in 2008: the French West Indies, the Netherlands Antilles, Anguilla, Antigua and Barbuda, Grenada, Trinidad and Tobago. In: Wilkinson C (ed) Status of the coral reefs of the world. Australian institute of marine sciences, Australia, pp 265–280

    Google Scholar 

  8. Bove CB, Ries JB, Davies SW, Westfield IT, Umbanhowar J, Castillo KD (2019) Common Caribbean corals exhibit highly variable responses to future acidification and warming. Proc Biol Sci 286. https://doi.org/10.1098/rspb.2018.2840

  9. Byler KA, Carmi-Veal M, Fine M, Goulet TL (2013) Multiple symbiont acquisition strategies as an adaptive mechanism in the coral Stylophora pistillata. Plos One 8. https://doi.org/10.1371/journal.pone.0059596

  10. Casano LM, Zapata JM, Martin M, Sabater B (2000) Chlororespiration and poising of cyclic electron transport - Plastoquinone as electron transporter between thylakoid NADH dehydrogenase and peroxidase. J Biol Chem 275:942–948

    CAS  PubMed  Google Scholar 

  11. Diaz JM, Hansel CM, Apprill A, Brighi C, Zhang T, Weber L, McNally S, Xun LP (2016) Species-specific control of external superoxide levels by the coral holobiont during a natural bleaching event. Nat Commun 7. https://doi.org/10.1038/ncomms13801

  12. Diaz-Almeyda EM, Prada C, Ohdera AH, Moran H, Civitello DJ, Iglesias-Prieto R, Carlo TA, LaJeunesse TC, Medina M (2017) Intraspecific and interspecific variation in thermotolerance and photoacclimation in Symbiodinium dinoflagellates. P Roy Soc B-Biol Sci 284. https://doi.org/10.1098/rspb.2017.1767

  13. Enriquez S, Mendez ER, Hoegh-Guldberg O, Iglesias-Prieto R (2017) Key functional role of the optical properties of coral skeletons in coral ecology and evolution. P Roy Soc B Biol Sci 284. https://doi.org/10.1098/rspb.2016.1667

  14. Franklin LA, Seaton GGR, Lovelock CE, Larkum AWD (1996) Photoinhibition of photosynthesis on a coral reef. Plant Cell Environ 19:825–836

    Google Scholar 

  15. Gardner TA, Cote IM, Gill JA, Grant A, Watkinson AR (2003) Long-term region-wide declines in Caribbean corals. Science 301:958–960

    CAS  PubMed  Google Scholar 

  16. Gardner SG, Raina JB, Ralph PJ, Petrou K (2017) Reactive oxygen species (ROS) and dimethylated sulphur compounds in coral explants under acute thermal stress. J Exp Biol 220:1787–1791

    PubMed  Google Scholar 

  17. Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron-transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92

    CAS  Google Scholar 

  18. Green DH, Edmunds PJ, Carpenter RC (2008) Increasing relative abundance of Porites astreoides on Caribbean reefs mediated by an overall decline in coral cover. Mar Ecol Prog Ser 359:1–10

    Google Scholar 

  19. Gregoire V, Schmacka F, Coffroth MA, Karsten U (2017) Photophysiological and thermal tolerance of various genotypes of the coral endosymbiont Symbiodinium sp (Dinophyceae). J Appl Phycol 29:1893–1905

    Google Scholar 

  20. Grottoli AG, Warner ME, Levas SJ, Aschaffenburg MD, Schoepf V, McGinley M, Baumann J, Matsui Y (2014) The cumulative impact of annual coral bleaching can turn some coral species winners into losers. Global Change Biol 20:3823–3833

    Google Scholar 

  21. Hauff B, Haslun JA, Strycha KB, Ostrom PH, Cervino JM (2016) Symbiont diversity of zooxanthellae (Symbiodinium spp.) in Porites astreoides and Montastraea cavernosa from a reciprocal transplant in the lower Florida Keys. Int J Biol 8:9–22

    Google Scholar 

  22. Hennige SJ, Suggett DJ, Warner ME, McDougall KE, Smith DJ (2009) Photobiology of Symbiodinium revisited: bio-physical and bio-optical signatures. Coral Reefs 28:179–195

    Google Scholar 

  23. Hill R, Ralph PJ (2008) Dark-induced reduction of the plastoquinone pool in zooxanthellae of scleractinian corals and implications for measurements of chlorophyll a fluorescence. Symbiosis 46:45–56

    CAS  Google Scholar 

  24. Hill R, Larkum AWD, Prasil O, Kramer DM, Szabo M, Kumar V, Ralph PJ (2012) Light-induced dissociation of antenna complexes in the symbionts of scleractinian corals correlates with sensitivity to coral bleaching. Coral Reefs 31:963–975

    Google Scholar 

  25. Houille-Vernes L, Rappaport F, Wollman F-A, Alric J, Johnson X (2011) Plastid terminal oxidase 2 (PTOX2) is the major oxidase involved in chlororespiration in Chlamydomonas. Proc Natl Acad Sci U S A 108:20820–20825

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Iglesias-Prieto R, Beltran VH, LaJeunesse TC, Reyes-Bonilla H, Thome PE (2004) Different algal symbionts explain the vertical distribution of dominant reef corals in the eastern Pacific. P Roy Soc B Biol Sci 271:1757–1763

    CAS  Google Scholar 

  27. Jans F, Mignolet E, Houyoux P-A, Cardol P, Ghysels B, Cuine S, Cournac L, Peltier G, Remacle C, Franck F (2008) A type II NAD(P) H dehydrogenase mediates light-independent plastoquinone reduction in the chloroplast of Chlamydomonas. Proc Natl Acad Sci U S A 105:20546–20551

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Japaud A (2017) Les coraux du genre Acropora sur les récifs des Petites Antilles: approches génétiques, écologiques et de conservation. PhD thesis, Université des Antilles, Pointe-à-Pitre, Guadeloupe, p 271

  29. Javier Gonzalez-Barrios F, Alvarez-Filip L (2018) A framework for measuring coral species-specific contribution to reef functioning in the Caribbean. Ecol Indic 95:877–886

    Google Scholar 

  30. 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 

  31. Kanazawa A, Blanchard GJ, Szabo M, Ralph PJ, Kramer DM (2014) The site of regulation of light capture in Symbiodinium: Does the peridinin-chlorophyll alpha-protein detach to regulate light capture? Biochim Biophys Acta 1837:1227–1234

    CAS  PubMed  Google Scholar 

  32. Khorobrykh SA, Ivanov BN (2002) Oxygen reduction in a plastoquinone pool of isolated pea thylakoids. Photosynth Res 71:209–219

    CAS  PubMed  Google Scholar 

  33. Khorobrykh S, Havurinne V, Mattila H, Tyystjärvi E (2020) Oxygen and ROS in photosynthesis. Plants 9:91. https://doi.org/10.3390/plants9010091

    CAS  Article  Google Scholar 

  34. Kromkamp JC, Forster RM (2003) The use of variable fluorescence measurements in aquatic ecosystems: differences between multiple and single turnover measuring protocols and suggested terminology. Eur J Phycol 38:103–112

    Google Scholar 

  35. Krueger T, Becker S, Pontasch S, Dove S, Hoegh-Guldberg O, Leggat W, Fisher PL, Davy SK (2014) Antioxidant plasticity and thermal sensitivity in four types of symbiodinium sp. J Phycol 50:1035–1047

    CAS  PubMed  Google Scholar 

  36. LaJeunesse TC (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar Biol 141:387–400

    Google Scholar 

  37. LaJeunesse TC, Smith R, Walther M, Pinzon J, Pettay DT, McGinley M, Aschaffenburg M, Medina-Rosas P, Cupul-Magana AL, Lopez Perez A, Reyes-Bonilla H, Warner ME (2010) Host-symbiont recombination versus natural selection in the response of coral-dinoflagellate symbioses to environmental disturbance. P Roy Soc B Biol Sci 277:2925–2934

    Google Scholar 

  38. 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 

  39. Lesser MP (1996) Elevated temperatures and ultraviolet radiation cause oxidative stress and inhibit photosynthesis in symbiotic dinoflagellates. Limnol Oceanogr 41:271–283

    CAS  Google Scholar 

  40. Lesser MP (2006) Oxidative stress in marine environments: Biochemistry and physiological ecology. Annu Rev Physiol 68:253–278

    CAS  PubMed  Google Scholar 

  41. Levas S, Schoepf V, Warner ME, Aschaffenburg M, Baumann J, Grottoli AG (2018) Long-term recovery of caribbean corals from bleaching. J Exp Mar Bio Ecol 506:124–134

    CAS  Google Scholar 

  42. Martin M, Sabater B (2010) Plastid ndh genes in plant evolution. Plant Physiol Bioch 48:636–645

    CAS  Google Scholar 

  43. McGinty ES, Pieczonka J, Mydlarz LD (2012) Variations in reactive oxygen release and antioxidant activity in multiple symbiodinium types in response to elevated temperature. Microb Ecol 64:1000–1007

    CAS  PubMed  Google Scholar 

  44. Nawrocki WJ, Tourasse NJ, Taly A, Rappaport F, Wollman FA (2015) The plastid terminal oxidase: its elusive function points to multiple contributions to plastid physiology. Annual review of plant biology 66:49–74

    CAS  PubMed  Google Scholar 

  45. Nawrocki WJ, Buchert F, Joliot P, Rappaport F, Bailleul B, Wollman F-A (2019) Chlororespiration controls growth under intermittent light. Plant Physiol 179:630–639

    CAS  PubMed  Google Scholar 

  46. Nielsen DA, Petrou K, Gates RD (2018) Coral bleaching from a single cell perspective. Isme J 12:1558–1567

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Nixon PJ (2000) Chlororespiration. P Roy Soc B Biol Sci 355:1541–1547

    CAS  Google Scholar 

  48. Peltier G, Schmidt GW (1991) Chlororespiration - an adaptation to nitrogen deficiency in chlamydomonas-reinhardtii. Proc Natl Acad Sci U S A 88:4791–4795

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Peltier G, Aro EM, Shikanai T (2016) NDH-1 and NDH-2 plastoquinone peductases in oxygenic photosynthesis. Annual review of plant biology 67:55–80

    CAS  PubMed  Google Scholar 

  50. Pochon X, Forsman ZH, Spalding HL, Padilla-Gamino JL, Smith CM, Gates RD (2015) Depth specialization in mesophotic corals (Leptoseris spp.) and associated algal symbionts in Hawaii. R Soc Open Sci 2. https://doi.org/10.1098/rsos.140351

  51. Ragni M, Airs RL, Hennige SJ, Suggett DJ, Warner ME, Geider RJ (2010) PSII photoinhibition and photorepair in Symbiodinium (Pyrrhophyta) differs between thermally tolerant and sensitive phylotypes. Mar Ecol Prog Ser 406:57–70

    CAS  Google Scholar 

  52. Ralph PJ, Gademann R, Dennison WC (1998) In situ seagrass photosynthesis measured using a submersible, pulse-amplitude modulated fluorometer. Mar Biol 132:367–373

    Google Scholar 

  53. Rehman AU, Szabo M, Deak Z, Sass L, Larkum A, Ralph P, Vass I (2016) Symbiodinium sp cells produce light-induced intra- and extracellular singlet oxygen, which mediates photodamage of the photosynthetic apparatus and has the potential to interact with the animal host in coral symbiosis. New Phytol 212:472–484

    CAS  PubMed  Google Scholar 

  54. Reynolds JM, Bruns BU, Fitt WK, Schmidt GW (2008) Enhanced photoprotection pathways in symbiotic dinoflagellates of shallow-water corals and other cnidarians. Proc Natl Acad Sci U S A 105:13674–13678

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Roberty S, Bailleul B, Berne N, Franck F, Cardol P (2014) PSI Mehler reaction is the main alternative photosynthetic electron pathway in Symbiodinium sp., symbiotic dinoflagellates of cnidarians. New Phytol 204:81–91

    CAS  PubMed  Google Scholar 

  56. Roberty S, Fransolet D, Cardol P, Plumier JC, Franck F (2015) Imbalance between oxygen photoreduction and antioxidant capacities in Symbiodinium cells exposed to combined heat and high light stress. Coral Reefs 34:1063–1073

    Google Scholar 

  57. Robison JD, Warner ME (2006) Differential impacts of photoacclimation and thermal stress on the photobiology of four different phylotypes of Symbiodinium (Pyrrhophyta). J Phycol 42:568–579

    CAS  Google Scholar 

  58. Romaine S, Tambutte E, Allemand D, Gattuso JP (1997) Photosynthesis, respiration and calcification of a zooxanthellate scleractinian coral under submerged and exposed conditions. Mar Biol 129:175–182

    Google Scholar 

  59. Rowan R, Knowlton N (1995) Intraspecific diversity and ecological zonation in coral algal symbiosis. Proc Natl Acad Sci U S A 92:2850–2853

    CAS  PubMed  PubMed Central  Google Scholar 

  60. Saroussi SI, Wittkopp TM, Grossman AR (2016) The type II NADPH dehydrogenase facilitates cyclic electron flow, energy-dependent quenching, and chlororespiratory metabolism during acclimation of Chlamydomonas reinhardtii to nitrogen deprivation. Plant Physiol 170:1975–1988

    CAS  PubMed  PubMed Central  Google Scholar 

  61. Saroussi S, Sanz-Luque E, Kim RG, Grossman AR (2017) Nutrient scavenging and energy management: acclimation responses in nitrogen and sulfur deprived Chlamydomonas. Curr Opin Plant Biol 39:114–122

    CAS  PubMed  Google Scholar 

  62. Schoepf V, Grottoli AG, Levas SJ, Aschaffenburg MD, Baumann JH, Matsui Y, Warner ME (2015) Annual coral bleaching and the long-term recovery capacity of coral. Proc. R. Soc. B 282:20151887. https://doi.org/10.1098/rspb.2015.1887

    CAS  Article  PubMed  Google Scholar 

  63. Scibilia L, Girolomoni L, Berteotti S, Alboresi A, Ballottari M (2015) Photosynthetic response to nitrogen starvation and high light in Haematococcus pluvialis. Algal Res 12:170–181

    Google Scholar 

  64. Serrano XM, Baums IB, Smith TB, Jones RJ, Shearer TL, Baker AC (2016) Long distance dispersal and vertical gene flow in the Caribbean brooding coral Porites astreoides. Sci Rep 6. https://doi.org/10.1038/srep21619

  65. Slavov C, Schrameyer V, Reus M, Ralph PJ, Hill R, Buchel C, Larkum AWD, Holzwarth AR (2016) “Super-quenching” state protects Symbiodinium from thermal stress - Implications for coral bleaching. Biochim Biophys Acta Bioenerg 1857:840–847

    CAS  Google Scholar 

  66. Suggett DJ, Warner ME, Smith DJ, Davey P, Hennige S, Baker NR (2008) Photosynthesis and production of hydrogen peroxide by Symbiodinium (Pyrrhophyta) phylotypes with different thermal tolerances. J Phycol 44:948–956

    CAS  PubMed  Google Scholar 

  67. Takahashi S, Whitney SM, Badger MR (2009) Different thermal sensitivity of the repair of photodamaged photosynthetic machinery in cultured Symbiodinium species. Proc Natl Acad Sci U S A 106:3237–3242

    CAS  PubMed  PubMed Central  Google Scholar 

  68. Tolleter D, Seneca FO, DeNofrio JC, Krediet CJ, Palumbi SR, Pringle JR, Grossman AR (2013) Coral bleaching independent of photosynthetic activity. Curr Biol 23:1782–1786

    CAS  PubMed  Google Scholar 

  69. Wangpraseurt D, Lichtenberg M, Jacques SL, Larkum AWD, Kuehl M (2019) Optical Properties of Corals Distort Variable Chlorophyll Fluorescence Measurements. Plant Physiol 179:1608–1619

    CAS  PubMed  PubMed Central  Google Scholar 

  70. Warner ME, LaJeunesse TC, Robison JD, Thur RM (2006) The ecological distribution and comparative photobiology of symbiotic dinoflagellates from reef corals in Belize: Potential implications for coral bleaching. Limnol Oceanogr 51:1887–1897

    Google Scholar 

  71. Wooldridge SA, Done TJ (2009) Improved water quality can ameliorate effects of climate change on corals. Ecol Appl 19:1492–1499

    PubMed  Google Scholar 

  72. Zhang T, Diaz JM, Brighi C, Parsons RJ, McNally S, Apprill A, Hansel CM (2016) Dark production of extracellular superoxide by the coral Porites astreoides and representative symbionts. Front Mar Sci 3. https://doi.org/10.3389/fmars.2016.00232

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Acknowledgements

This work was supported by funds from UMR BOREA, and the works done by P. Claquin and P.J. Lopez were co-funded by the Labex DRIIHM, French program “Investissements d’Avenir” (ANR-11-LABX-0010), managed by the ANR, and the OHM Littoral Caraïbe.

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Supplementary Fig 1.

Dynamics of F (black circle), Fm or Fm’ (white circle) in A: Acropora palmata, B: Agaricia agaricites, C: Orbicella annularis, D: Orbicella faveolata, E: Porites divaricata, F: Porites furcata, G: Pseudodiploria clivosa, H: Siderastrea siderea, during light dark transitions (dotted line: PAR).

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Claquin, P., Rene-Trouillefou, M., Lopez, P.J. et al. Singular physiological behavior of the scleractinian coral Porites astreoides in the dark phase. Coral Reefs 40, 139–150 (2021). https://doi.org/10.1007/s00338-020-02023-4

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Keywords

  • Chlororespiration-like
  • PAM
  • Caribbean reef corals
  • Resilience