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Gene expression in the scleractinian Acropora microphthalma exposed to high solar irradiance reveals elements of photoprotection and coral bleaching

Background: The success of tropical reef-building corals depends on the metabolic co-operation between the animal host and the photosynthetic performance of endosymbiotic algae residing within its cells. Dysfunction of coral symbiosis can occur under conditions of abnormally elevated water temperatures in combination with high light exposure causing the expulsion of endosymbionts or loss of algal pigments that is evinced as “coral bleaching”. Methodology/Principal Findings: To examine the molecular response of the coral Acropora microphthalma to high levels of solar irradiance, a cDNA library was constructed by PCR-based suppression subtractive hybridisation (PCR-SSH) from mRNA obtained by transplantation of a colony from a depth of 12.7 m to near-surface solar irradiance, during which the coral paled noticeably in sun-exposed tissues. The PCR-SSH cDNA library gave genetic evidence for a hypothetical biosynthetic pathway branching from the shikimic acid pathway and leading to the formation of 4-deoxygadusol, a potent antioxidant and direct precursor of the UV-protective mycosporine-like amino acids (MAAs), which serve as sunscreens in coral phototrophic symbiosis. Empirical PCR-based evidence further upholds the contention that the biosynthesis of these MAA sunscreens is a ‘shared metabolic adaptation’ between the symbiotic partners. Additionally, gene expression induced by enhanced solar irradiance reveals a cellular mechanism of light-induced coral bleaching that invokes a Ca-binding synaptotagmin-like regulator of SNARE protein assembly of phagosomal exocytosis, whereby algal partners are lost from the symbiosis. Conclusions/Significance: A novel approach to gene annotation in a coral, a non-model organism for which there are limited genetic data, is presented that provides evidence of genes encoding a MAA biosynthetic pathway and also identifies other genes that implicate exocytosis as a possible mechanism leading to a breakdown in the metabolically essential partnership between the coral host and endosymbiotic algae manifested as coral bleaching.

Cnidaria; symbiosis; photoprotection; mycosporine-like amino acids; coral bleaching; exocytosis

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