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Coral Reefs

, Volume 33, Issue 2, pp 513–522 | Cite as

Nitric oxide and heat shock protein 90 co-regulate temperature-induced bleaching in the soft coral Eunicea fusca

  • Cliff Ross
Report

Abstract

Coral bleaching represents a complex physiological process that is affected not only by environmental conditions but by the dynamic internal cellular biology of symbiotic dinoflagellates (Symbiodinium spp.) and their cnidarian hosts. Recently, nitric oxide (NO) has emerged as a key molecule involved with the expulsion of Symbiodinium from host cnidarian cells. However, the site of production remains under debate, and the corresponding signaling pathways within and between host and endosymbiont remain elusive. In this study, using freshly isolated Symbiodinium from the soft coral Eunicea fusca, I demonstrate that thermally induced stress causes an upregulation in Symbiodinium heat shock protein 90 (Hsp90). In turn, Hsp90 shows a concomitant ability to enhance the activity of a constitutively expressed isoform of NO synthase. The resulting production of NO constitutes a signaling molecule capable of inducing Symbiodinium expulsion. Using nitric oxide synthase (NOS) and Hsp90 polyclonal antibodies, thermal stress-induced Hsp90 was shown to co-immunoprecipitate with a constitutive isoform of NOS. The specific blocking of Hsp90 activity, with the Hsp90 inhibitor geldanamycin, was capable of inhibiting NO production implicating the involvement of a coordinated regulatory system. These results have strong evolutionary implications for Hsp90–NOS chaperone complexes among biological kingdoms and provide evidence for a new functional role in symbiotic associations.

Keywords

Coral bleaching Heat shock protein Nitric oxide Symbiodinium Symbiosis 

Notes

Acknowledgments

This work was supported by a Smithsonian Institution postdoctoral fellowship at the Smithsonian Marine Station at Ft. Pierce. I gratefully acknowledge Dr. Lory Z. Santiago-Vazquez for collection of E. fusca colonies and guidance isolating Symbiodinium. I also thank Valerie Paul, Raphael Ritson-Williams, Sherry Reed, Hugh Reichardt, Julie Piraino, Joan Kaminski, and Woody Lee from the Smithsonian Marine Station at Ft. Pierce for their invaluable support. This is contribution #944 of the Smithsonian Marine Station at Ft. Pierce.

References

  1. Anthony KRN, 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 USA 105:17442–17446PubMedCentralPubMedCrossRefGoogle Scholar
  2. Arasimowicz-Jelonek M, Floryszak-Wieczorek J (2011) Understanding the fate of peroxynitrite in plant cells-from physiology to pathophysiology. Phytochemistry 72:681–688PubMedCrossRefGoogle Scholar
  3. Bender AT, Nakatsuka M, Osawa Y (2000) Heme insertion, assembly, and activation of apo-neuronal nitric-oxide synthase in vitro. J Biol Chem 275:26018–26023PubMedCrossRefGoogle Scholar
  4. Bender AT, Silverstein AM, Demady DR, Kanelakis KC, Noguchi S, Pratt WC, Osawa Y (1999) Neuronal nitric oxide synthase is regulated by the hsp90-based chaperone system in vivo. J Biol Chem 274:1472–1478PubMedCrossRefGoogle Scholar
  5. Bishop CD, Brandhorst BP (2001) NO/cGMP signaling and HSP90 activity represses metamorphosis in the sea urchin Lytechinus pictus. Biol Bull 201:394–404PubMedCrossRefGoogle Scholar
  6. Bishop CD, Bates WR, Brandhorst BP (2001) Regulation of metamorphosis in ascidians involves NO/cGMP signaling and HSP90. J Exp Zool 289:374–384PubMedCrossRefGoogle Scholar
  7. Bouchard JN, Yamasaki H (2008) Heat stress stimulates nitric oxide production in Symbiodinium microadriaticum: A possible linkage between nitric oxide and the coral bleaching phenomenon. Plant Cell Physiol 49:641–652PubMedCrossRefGoogle Scholar
  8. Davidson SK, Koropatnick TA, Kossmehl R, Sycuro L, McFall-Nqai MJ (2004) NO means ‘yes’ in the squid-vibrio symbiosis: nitric oxide (NO) during the initial stages of a beneficial association. Cell Microbiol 6:1139–1151PubMedCrossRefGoogle Scholar
  9. Davy SK, Allemand D, Weis VM (2012) The cell biology of cnidarian–dinoflagellate symbiosis. Microbiol Mol Biol Rev 76:229–261PubMedCentralPubMedCrossRefGoogle Scholar
  10. del Rio LA, Corpas FJ, Barroso JB (2004) Nitric oxide and nitric oxide synthase activity in plants. Phytochemistry 65:783–792PubMedCrossRefGoogle Scholar
  11. DeSalvo MK, Sunagawa S, Voolstra CR, Medina M (2010) Transcriptomic responses to heat stress and bleaching in the elkhorn coral Acropora palmata. Mar Ecol Prog Ser 402:97–113CrossRefGoogle Scholar
  12. Desalvo MK, Voolstra CR, Sunagawa S, Schwarz JA, Stillman JH, Coffroth MA, Szmant AM, Medina M (2008) Differential gene expression during thermal stress and bleaching in the Caribbean coral Montastraea faveolata. Mol Ecol 17:3952–3971PubMedCrossRefGoogle Scholar
  13. Duque-Alarcon A, Santiago-Vazquez LZ, Kerr RG (2012) A microbial community analysis of the octocoral Eunicea fusca. Electron J Biotechn [doi:  10.2225/vol15-issue5-fulltext-11]
  14. Edge SE, Morgan MB, Gleason DF, Snell TW (2005) Development of a coral cDNA array to examine gene expression profiles in Montastraea faveolata exposed to environmental stress. Mar Pollut Bull 51:507–523PubMedCrossRefGoogle Scholar
  15. Fang L, Huang S, Lin K (1997) High temperature induces the synthesis of heat-shock proteins and the elevation of intracellular calcium in the coral Acropora grandis. Coral Reefs 16:127–131CrossRefGoogle Scholar
  16. Fitt WK, Gates RD, Hoegh-Guldberg O, Bythell JC, Jatkard A, Grottoli AG, Gomez M, Fisher P, Lajuenesse TC, Pantos O, Iglesias-Prieto R, Franklin DJ, Rodrigues LJ, Torregiani JM, van Woesik R, Lesser MP (2009) Response of two species of Indo- Pacific corals, Porites cylindrica and Stylophora pistillata, to short-term thermal stress: the host does matter in determining the tolerance of corals to bleaching. J Exp Mar Biol Ecol 373:102–110CrossRefGoogle Scholar
  17. Fleming I, Busse R (2003) Molecular mechanisms involved in the regulation of the endothelial nitric oxide synthase. Am J Physiol 284:R1–R12CrossRefGoogle Scholar
  18. Franklin DJ, Hoegh-Guldberg O, Jones RJ, Berges JA (2004) Cell death and degeneration in the symbiotic dinoflagellates of the coral Stylophora pistilla during bleaching. Mar Ecol Prog Ser 272:117–130CrossRefGoogle Scholar
  19. Frohlich A, Durner J (2011) The hunt for plant nitric oxide synthase (NOS): is one really needed? Plant Sci 181:401–404PubMedCrossRefGoogle Scholar
  20. Fulton D, Gratton JP, Sessa WC (2001) Post-translational control of endothelial nitric oxide synthase: why isn’t calcium/calmodulin enough? J Pharmacol Exp Ther 299:818–824PubMedGoogle Scholar
  21. Garcia-Cardena G, Fan R, Shah V, Sorrentino R, Cirino G, Papapetropoulos A, Sessa WC (1998) Dynamic activation of endothelial nitric oxide synthase by Hsp90. Nature 392:821–824PubMedCrossRefGoogle Scholar
  22. Gardner TA, Cote IM, Gill JA, Grant A, Watkinson AR (2003) Long term region wide declines in Caribbean corals. Science 301:958–960PubMedCrossRefGoogle Scholar
  23. Griffith OW, Kilbourn RG (1996) Nitric oxide synthase inhibitors: Amino acids. Methods Enzymol 268:375–392PubMedCrossRefGoogle Scholar
  24. Guo R, Ki JS (2012) Differential transcription of heat shock protein 90 (HSP90) in the dinoflagellate Prorocentrum minimum by copper and endocrine-disrupting chemicals. Ecotoxicology 21:1448–1457PubMedCrossRefGoogle Scholar
  25. Halliwell B (2006) Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol 141:312–322PubMedCentralPubMedCrossRefGoogle Scholar
  26. Hawkins TD, Davy SK (2012) Nitric oxide production and tolerance differ among Symbiodinium types exposed to heat stress. Plant Cell Physiol 53:1889–1898PubMedCrossRefGoogle Scholar
  27. Hawkins TD, Davy SK (2013) Nitric oxide and coral bleaching: is peroxynitrite generation required for symbiosis collapse? J Exp Biol 216:3185–3188PubMedCrossRefGoogle Scholar
  28. Hawkins TD, Bradley BJ, Davy SK (2013) Nitric oxide mediates coral bleaching through an apoptotic-like cell death pathway: evidence from a model sea anemone-dinoflagellate symbiosis. FASEB J [FASEB J fj.13-235051]Google Scholar
  29. Hentschel U, Steinert M, Hacker J (2000) Common molecular mechanisms of symbiosis and pathogenesis. Trends in Microbiol 8:226–231CrossRefGoogle Scholar
  30. Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866CrossRefGoogle Scholar
  31. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742PubMedCrossRefGoogle Scholar
  32. Iglesias-Prieto R, Trench RK (1997) Acclimation and adaptation to irradiance in symbiotic dinoflagellates. II. Response of chlorophyll-protein complexes to different photon-flux densities. Mar Biol 130:23–33CrossRefGoogle Scholar
  33. Ilangovan G, Osinbowale S, Bratasz A, Bonar M, Cardounel AJ, Zweier JL, Kuppusamy P (2004) Heat shock regulates the respiration of cardiac H9c2 cells through upregulation of nitric oxide synthase. Am J Physiol Cell Physiol 287:C1472–C1481PubMedCrossRefGoogle Scholar
  34. IPCC (2007) 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, Cambridge, UK and New York, NYGoogle Scholar
  35. Jacobson PB, Jacobs RS (1992) Fuscoside: An anti-inflammatory marine natural product which selectively inhibits 5-lipoxygenase. Part I: Physiological and biochemical studies in murine inflammatory models. J Pharmacol Exp Ther 262:866–873PubMedGoogle Scholar
  36. Jones RJ, Hoegh-Guldberg O, Larkum AWD, Schreiber U (1998) Temperature-induced bleaching of corals begins with impairment of the CO2 fixations mechanism in zooxanthellae. Plant Cell Environ 21:1219–1230CrossRefGoogle Scholar
  37. Kadota Y, Shirasu K (2012) The Hsp90 complex of plants. Biochim Biophys Acta 1823:689–697PubMedCrossRefGoogle Scholar
  38. Kingsley RJ, Afif E, Cox BC, Kothari S, Kriechbaum K, Kuchinsky K, Neill AT, Puri AF, Kish VM (2003) Expression of heat shock and cold shock proteins in the gorgonian Leptogorgia virgulata. J Exp Zool A Comp Exp Biol 296:98–107PubMedCrossRefGoogle Scholar
  39. Leggat W, Seneca F, Wasmund K, Ukani L, Yellowlees D, Ainsworth TD (2011) Differential responses of the coral host and their algal symbiont to thermal stress. PLoS ONE 6(10):e26687PubMedCentralPubMedCrossRefGoogle Scholar
  40. Lesser MP (2006) Oxidative stress in marine environments: Biochemistry and physiological ecology. Annu Rev Physiol 68:253–278PubMedCrossRefGoogle Scholar
  41. Li J, Buchner J (2013) Structure, function and regulation of the Hsp90 machinery. Biomed J 36:106–117PubMedCrossRefGoogle Scholar
  42. Mayfield AB, Wang L, Tang P, Fan T, Hsiao Y, Tsai C, Chen C (2011) Assessing the impacts of experimentally elevated temperature on the biological composition and molecular chaperone gene expression of a reef coral. PLoS ONE 6(10):e26529PubMedCentralPubMedCrossRefGoogle 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 64:1000–1007PubMedCrossRefGoogle Scholar
  44. Meilhoc E, Boscari A, Bruand C, Puppo A, Brouquisse R (2011) Nitric oxide in legume-rhizobium symbiosis. Plant Sci 181:573–581PubMedCrossRefGoogle Scholar
  45. Mittal CK, Jadhav AL (1994) Calcium-dependent inhibition of constitutive nitric oxide synthase. Biochem Biophys Res Commun 30:8–15CrossRefGoogle Scholar
  46. Mur LAJ, Mandon J, Persijn S, Cristescu SM, Moshkov IE, Novikova GV, Hall MA, Harren FJM, Hebelstrup KH, Gupta KJ (2013) Nitric oxide in plants: an assessment of the current state of knowledge. AoB PLANTS 5: pls052Google Scholar
  47. Mydlarz LD, Jacobs RS (2006) An inducible release of reactive oxygen species of gorgonian corals. Mar Freshw Behav Physiol 39:143–152CrossRefGoogle Scholar
  48. Palumbo A (2005) Nitric oxide in marine invertebrates: a comparative perspective. Comp Biochem Physiol Part A Mol Integr Physiol 142:241–248CrossRefGoogle Scholar
  49. Perez S, Weis VM (2006) Nitric oxide and cnidarian bleaching: an eviction notice mediates breakdown of a symbiosis. J Exp Biol 209:2804–2810PubMedCrossRefGoogle Scholar
  50. Perez SF, Cook CB, Brooks WR (2001) The role of symbiotic dinoflagellates in the temperature-induced bleaching response of the subtropical sea anemone Aiptasia pallida. J Exp Mar Biol Ecol 256:1–14PubMedCrossRefGoogle Scholar
  51. Polato NR, Voolstra CR, Schnetzer J, DeSalvo MK, Randall CJ, Szmant AM, Medina M, Baums IB (2010) Location-specific responses to thermal stress in larvae of the reef-building coral Montastraea faveolata. PLoS ONE 5(6):e11221PubMedCentralPubMedCrossRefGoogle Scholar
  52. Rasher DB, Hay ME (2010) Chemically rich seaweeds poison corals when not controlled by herbivores. Proc Natl Acad Sci USA 107:9683–9688PubMedCentralPubMedCrossRefGoogle Scholar
  53. Robbart ML, Peckol P, Scordilis SP, Curran HA, Brown-Saracino J (2004) Population recovery and differential heat shock protein expression for the corals Agaricia agaricites and A. tenuifolia in Belize. Mar Ecol Prog Ser 283:151–160CrossRefGoogle Scholar
  54. Rodriguez-Lanetty M, Harii S, Hoegh-Guldberg O (2009) Early molecular responses of coral larvae to hyperthermal stress. Mol Ecol 18:5101–5114PubMedCrossRefGoogle Scholar
  55. Rosic N, Pernice M, Dove S, Dunn S, Hoegh-Guldberg O (2011a) Gene expression profiles of cytosolic heat shock proteins Hsp70 and Hsp90 from symbiotic dinoflagellates in response to thermal stress: possible implications for coral bleaching. Cell Stress Chaperones 16:69–80PubMedCentralPubMedCrossRefGoogle Scholar
  56. Rosic NN, Pernice M, Rodriguez-Lanetty M, Hoegh-Guldberg O (2011b) Validation of housekeeping genes for gene expression studies in Symbiodinium exposed to thermal and light stress. Mar Biotechnol 13:355–365PubMedCrossRefGoogle Scholar
  57. Ross C, Küpper FC, Jacobs RS (2006) Involvement of reactive oxygen species and reactive nitrogen species in the wound response in Dasycladus vermicularis (Chlorophyta). Chem Biol 13:353–364PubMedCrossRefGoogle Scholar
  58. Safavi-Hemami H, Young ND, Doyle J, Llewellyn L, Klueter A (2010) Characterisation of nitric oxide synthase in three cnidarian-dinoflagellate symbioses. PLoS ONE 5(4):e10379PubMedCentralPubMedCrossRefGoogle Scholar
  59. Sangster TA, Queitsch C (2005) The HSP90 chaperone complex, an emerging force in plant development and phenotypic plasticity. Curr Opin Plant Biol 8:86–92PubMedCrossRefGoogle Scholar
  60. Sharp VA, Brown BE, Miller D (1997) Heat shock protein (hsp 70) expression in the tropical reef coral Goniopora djiboutiensis. J Therm Biol 22:11–19CrossRefGoogle Scholar
  61. Sheppard C, Rioja-Nieto R (2005) Sea surface temperature1871–2099 in 38 cells in the Caribbean region. Mar Environ Res 60:389–396PubMedCrossRefGoogle Scholar
  62. Shin J, Fenical W (1991) Fuscosides A-D: antiinflammatory diterpenoid glycosides of new structural classes from the Caribbean gorgonian Eunicia fusca. J Org Chem 56:3153–3158CrossRefGoogle Scholar
  63. Suggett DJ, Warner ME, Smith DJ, Davey P, Hennige SJ, Baker NR (2008) Photosynthesis and production of hydrogen peroxide by Symbiodinium (Pyrrhophyta) phylotypes with different thermal tolerances. J Phycol 44:948–956CrossRefGoogle Scholar
  64. Tchernov D, Gorbunov MY, de Vargas C, Yadav SN, Milligan AJ, Haggblom M, Falkowski PG (2004) Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proc Natl Acad Sci USA 101:13531–13535PubMedCentralPubMedCrossRefGoogle Scholar
  65. Trapido-Rosenthal HG, Sharp KH, Galloway TS, Morrall CE (2001) Nitric oxide and cnidarian–dinoflagellate symbioses: pieces of a puzzle. Am Zool 41:247–257CrossRefGoogle Scholar
  66. Ueda N, Degnan SM (2013) Nitric oxide acts as a positive regulator to induce metamorphosis of the ascidian Herdmania momus. PLoS ONE 8(9):e72797PubMedCentralPubMedCrossRefGoogle Scholar
  67. Voolstra CR, Schnetzer J, Peshkin L, Randall CJ, Szmant AM, Medina M (2009) Effects of temperature on gene expression in embryos of the coral Montastraea faveolata. BMC Genomics 10:627PubMedCentralPubMedCrossRefGoogle Scholar
  68. Wang Y, Ruby EG (2011) The roles of NO is microbial symbioses. Cell Microbiol 13:518–526PubMedCentralPubMedCrossRefGoogle Scholar
  69. Warner ME, Fitt WK, Schmidt GW (1999) Damage to photosystem II in symbiotic dinoflagellates: a determinant of coral bleaching. Proc Natl Acad Sci USA 96:8007–8012PubMedCentralPubMedCrossRefGoogle Scholar
  70. Weis VM (2008) Cellular mechanisms of cnidarian bleaching: stress causes the collapse of symbiosis. J Exp Biol 211:3059–3066PubMedCrossRefGoogle Scholar
  71. Yoshida M, Xia Y (2003) Heat shock protein 90 as an endogenous protein enhancer of inducible nitric-oxide synthase. J Biol Chem 278:36953–36958PubMedCrossRefGoogle Scholar
  72. Zhao R, Houry WA (2007) Molecular interaction network of the Hsp90 chaperone system. Adv Exp Med Biol 594:27–36PubMedCrossRefGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.Department of Biological SciencesUniversity of North FloridaJacksonvilleUSA

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