Abstract

The stability of cnidarian-dinoflagellate endosymbioses is dependent upon communication between the host gastrodermal cell and the symbionts housed within it. Although the molecular mechanisms remain to be elucidated, existing evidence suggests that the establishment of these endosymbioses may involve the sorting of membrane proteins. The present study examined the role of host gastrodermal membranes in regulating symbiont (genus Symbiodinium) photosynthesis in the stony coral Euphyllia glabrescens. In comparison with the photosynthetic behavior of Symbiodinium in culture, the Symbiodinium populations within isolated symbiotic gastrodermal cells (SGCs) exhibited a significant degree of photo-inhibition, as determined by a decrease in the photochemical efficiency of photosystem II (F (v)/F (m)). This photo-inhibition coincided with increases in plasma membrane perturbation and oxidative activity in the SGCs. Membrane trafficking in SGCs was examined using the metabolism of a fluorescent lipid analog, N-[5-(5,7-dimethyl boron dipyrromethene difluoride)-1-pentanoyl]-D-erythro-Sphingosylphosphoryl-choline (BODIPY-Sphingomyelin or BODIPY-SM). Light irradiation altered both membrane distribution and trafficking of BODIPY-SM, resulting in metabolic changes. Cholesterol depletion of the SGC plasma membranes by methyl-β-cyclodextrin retarded BODIPY-SM degradation and further augmented Symbiodinium photo-inhibition. These results indicate that Symbiodinium photo-inhibition may be related to perturbation of the host gastrodermal membrane, providing evidence for the pivotal role of host membrane trafficking in the regulation of this environmentally important coral-dinoflagellate endosymbiosis.

Highlights

  • Cnidarian-dinoflagellate endosymbioses, in which gastrodermal cells of the host animal harbor photosynthetic dinoflagellates (i.e., Symbiodinium sp.), are of mutual benefit to both partners, yet are prone to disintegration upon prolonged exposure to environmental changes [1]

  • Cholesterol depletion of the symbiotic gastrodermal cells (SGCs) plasma membranes by methyl- -cyclodextrin retarded BODIPY-symbiosome membranes (SM) degradation and further augmented Symbiodinium photo-inhibition. These results indicate that Symbiodinium photo-inhibition may be related to perturbation of the host gastrodermal membrane, providing evidence for the pivotal role of host membrane trafficking in the regulation of this environmentally important coral-dinoflagellate endosymbiosis

  • Isolated SGCs contain single to multiple numbers of clade C1 Symbiodinium

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Summary

Introduction

Cnidarian-dinoflagellate endosymbioses, in which gastrodermal cells of the host animal harbor photosynthetic dinoflagellates (i.e., Symbiodinium sp.), are of mutual benefit to both partners, yet are prone to disintegration upon prolonged exposure to environmental changes [1]. Most phagosomes containing either heat-killed or photosynthetically-impaired Symbiodinium tested positive for Rab-7 These data indicate that development and regulation of endosymbiosis involves highly coordinated membrane trafficking between the host plasma membrane, the phagosome membrane, and the symbiosome membrane [4]. Past studies have shown that Symbiodinium thylakoid membrane lipids are damaged in corals undergoing thermal stressinduced bleaching [14]. These authors found that different lipid ratios of various Symbiodinium clones correlated with their response to environmental stress, as reflected by photochemical efficiency changes. It is highly possible that irradiation may affect photosynthesis, and perturb the membrane composition or metabolism in both components of the cnidariandinoflagellate holobiont

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