Nitric oxide and heat shock protein 90 co-regulate temperature-induced bleaching in the soft coral Eunicea fusca
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.
KeywordsCoral bleaching Heat shock protein Nitric oxide Symbiodinium Symbiosis
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.
- 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]
- 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
- 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
- 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
- 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
- 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
- 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