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

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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.

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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.

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Correspondence to Cliff Ross.

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Ross, C. Nitric oxide and heat shock protein 90 co-regulate temperature-induced bleaching in the soft coral Eunicea fusca . Coral Reefs 33, 513–522 (2014). https://doi.org/10.1007/s00338-014-1142-5

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