Apoptosis and the selective survival of host animals following thermal bleaching in zooxanthellate corals

Abstract

During the past several decades, numerous reports from disparate geographical areas have documented an increased frequency of "bleaching" in reef-forming corals. The phenomenon, triggered by increased sea surface temperatures, occurs when the cnidarian hosts digest and/or expel their intracellular, photosynthetic dinoflagellate symbionts ("zooxanthellae" in the genus Symbiodinium). Although coral bleaching is often followed by the death of the animal hosts, in some cases, the animal survives and can be repopulated with viable zooxanthellae. The physiological factors determining the ability of the coral to survive bleaching events are poorly understood. In this study, we experimentally established that bleaching and death of the host animal involve a caspase-mediated apoptotic cascade induced by reactive oxygen species produced primarily by the algal symbionts. In addition, we demonstrate that, although some corals naturally suppress caspase activity and significantly reduce caspase concentration under high temperatures as a mechanism to prevent colony death from apoptosis, even sensitive corals can be prevented from dying by application of exogenous inhibitors of caspases. Our results indicate that variability in response to thermal stress in corals is determined by a four-element, combinatorial genetic matrix intrinsic to the specific symbiotic association. Based on our experimental data, we present a working model in which the phenotypic expression of this symbiont/host relationship places a selective pressure on the symbiotic association. The model predicts the survival of the host animals in which the caspase-mediated apoptotic cascade is down-regulated.

Evolution of TNF-induced apoptosis reveals 550 My of functional conservation

“…2F). A biochemical model of bleaching has been proposed in which reactive oxygen species (ROS) production by the algal symbionts compromises the structural integrity of the mitochondrial membrane, stimulating the release of apoptotic factors and caspase activation (43). With the identification of a diverse repertoire of 40 putative TNF receptors and 13 putative TNF ligands described here, as well as the potential involvement of the mitochondria on HuTNFα exposure (Fig.…”

Breakdown of coral colonial form under reduced pH conditions is initiated in polyps and mediated through apoptosis

“…Caspase activity was assayed fluorometrically from each fragment/tissue, using the specific substrate Ac-DEVD-AFC (N-acetyl-Asp-GluVal-Asp-7-amido-4-trifluoromethylcoumarin) (Calbiochem), as described (15). Caspase activity was expressed as relative fluorescence units/μg protein −1 ·h −1 .…”

“…Apoptosis has been remarkably well-conserved within metazoan phyla, both in terms of morphologic cellular features and in the repertoire of genes involved. The presence of appropriate cellular and molecular machinery in Anthozoa has been established (11); however, the involvement of this mechanism after stress events is still unclear (12)(13)(14)(15). In corals, regulated, tissuespecific apoptosis after thermal stress has been experimentally established (14,15), and its induction/reduction in the coral tissues matched the profiles of caspase-3 activity and caspase-3 gene expression (14).…”

“…The presence of appropriate cellular and molecular machinery in Anthozoa has been established (11); however, the involvement of this mechanism after stress events is still unclear (12)(13)(14)(15). In corals, regulated, tissuespecific apoptosis after thermal stress has been experimentally established (14,15), and its induction/reduction in the coral tissues matched the profiles of caspase-3 activity and caspase-3 gene expression (14). Under reduced pH conditions, changes in apoptosis-related gene expression, including up-regulation of caspase 3, were reported for the stony coral Acropora millepora (16).…”

Corals from the Persian/Arabian Gulf as models for thermotolerant reef-builders: Prevalence of clade C3 Symbiodinium, host fluorescence and ex situ temperature tolerance

“…When the visual appearance of the coral becomes dominated by the white colour of the skeleton showing through the tissue, the phenomenon is known as ''bleaching''. Bleaching due to thermal stress is considered to be induced by the algal production of reactive oxygen species (ROS), particularly H 2 O 2 (Lesser, 2006;Smith et al, 2005;Suggett et al, 2008;Tchernov et al, 2011). Although the animal host might survive and recover, mass mortality is frequently observed among bleached corals Glynn, 1996;Wilkinson, 1998).…”