Abstract

BackgroundThe 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. 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 became noticeably paler from loss of endosymbionts in sun-exposed tissues.Methodology/Principal FindingsA novel approach to sequence annotation of the cDNA library gave genetic evidence for a hypothetical biosynthetic pathway branching from the shikimic acid pathway that leads to the formation of 4-deoxygadusol. This metabolite is a potent antioxidant and expected 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 Ca2+-binding synaptotagmin-like regulator of SNARE protein assembly of phagosomal exocytosis, whereby algal partners are lost from the symbiosis.Conclusions/SignificanceBioinformatics analyses of DNA sequences obtained by differential gene expression of a coral exposed to high solar irradiance has revealed the identification of putative genes encoding key steps of the MAA biosynthetic pathway. Revealed also by this treatment are genes that implicate exocytosis as a cellular process contributing to a breakdown in the metabolically essential partnership between the coral host and endosymbiotic algae, which manifests as coral bleaching.

Highlights

  • Reef-building corals (Anthozoa: Scleractinia) that typically inhabit the nutrient-poor and shallow waters of tropical marine ecosystems accommodate dense populations of endosymbiotic dinoflagellates of the genus Symbiodinium, which is divided into distinct sub-generic lineages

  • Annotation of cDNA sequences derived from A. microphthalma exposed to high solar irradiance

  • The PCR-based suppression subtractive hybridisation (PCR-SSH) cDNA library of genes up-regulated by the coral A. microphthalma contained 142 sequenced clones with inserts of a median sequence length of 396 bp

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Summary

Introduction

Reef-building corals (Anthozoa: Scleractinia) that typically inhabit the nutrient-poor and shallow waters of tropical marine ecosystems accommodate dense populations of endosymbiotic dinoflagellates of the genus Symbiodinium (known colloquially as zooxanthellae), which is divided into distinct sub-generic lineages (clades A–D). This phototrophic association allows the release of organic carbon produced by the algal partner for coral nutrition while metabolic wastes from the animal are recycled to fertilize algal photosynthesis [1]. 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 became noticeably paler from loss of endosymbionts in sun-exposed tissues

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