Photosynthetic and respiratory responses to thermal stress in the coral symbiont Symbiodinium

Abstract

The symbiotic algae of corals, dinoflagellates of the genus Symbiodinium, exist in a harsh environment characterized by high temperatures, hyperoxia, ultraviolet radiation and irradiance. Despite these stressors, Symbiodinium is able to fix inorganic carbon with an apparently inferior Form II Rubisco and metabolically drive one of the earth's most diverse and productive ecosystems. Coral reefs are threatened by coral bleaching, a physiological response characterized by the death or expulsion of the algal symbionts, which has been increasing in frequency in recent decades. As the coral mutualism is based upon the exchange of carbon, the effects of thermal stress on the carbon concentrating mechanism and photosynthetic parameters of cultured Symbiodinium were assayed. A novel apparatus was devised to simultaneously measure dissolved inorganic carbon and O2 flux while simultaneously measuring photosynthetic electron transport via PAM fluorometry in small algal culture samples. There has been considerable debate whether the initial point of thermal damage during high temperature coral bleaching is in the photosynthetic apparatus or in the “dark reactions” of the Calvin-Benham-Bassham cycle. Surprisingly, the inorganic carbon requirement for maximal photosynthetic and electron transport rates was found to be reduced in Symbiodinium cultures at high temperatures, with no evidence to support damage to Rubisco or carbon fixation. High inorganic carbon levels were found to be photoprotective, implying that inorganic carbon supply by the host is central for stabilizing the symbiosis. The hyperoxic conditions of coral tissues in the light combined with high temperatures and ultraviolet radiation are conducive to the formation of damaging reactive oxygen species (ROS). Excessive generation and release of ROS by symbionts in warm conditions triggers the coral bleaching response. Here, a mitochondrial terminal alternative oxidase, widespread among plants, was detected by inhibitor assay and transcriptome analysis and described for the first time in Symbiodinium cultures. Acclimation to both high and low temperatures induced greater terminal alternative oxidase capacity, which likely has a role in mitigating mitochondrial ROS generation. High affinity for inorganic carbon and enhanced mitochondrial alternative oxidase activity of Symbiodinium are demonstrated mechanisms by which these algae are capable of maintaining physiological function under thermal stress.