Regulation of Apoptotic Mediators Reveals Dynamic Responses to Thermal Stress in the Reef Building Coral Acropora millepora

Abstract

BackgroundMass coral bleaching is increasing in scale and frequency across the world's coral reefs and is being driven primarily by increased levels of thermal stress arising from global warming. In order to understand the impacts of projected climate change upon corals reefs, it is important to elucidate the underlying cellular mechanisms that operate during coral bleaching and subsequent mortality. In this respect, increased apoptotic cell death activity is an important cellular process that is associated with the breakdown of the mutualistic symbiosis between the cnidarian host and their dinoflagellate symbionts.Methodology/Principal FindingsThe present study reports the impacts of different stressors (colchicine and heat stress) on three phases of apoptosis: (i) the potential initiation by differential expression of Bcl-2 members, (ii) the execution of apoptotic events by activation of caspase 3-like proteases and (iii) and finally, the cell disposal indicated by DNA fragmentation in the reef building coral Acropora millepora. In corals incubated with colchicine, an increase in caspase 3-like activity and DNA fragmentation was associated with a relative down-regulation of Bcl-2, suggesting that the initiation of apoptosis may be mediated by the suppression of an anti-apoptotic mechanism. In contrast, in the early steps of heat stress, the induction of caspase-dependent apoptosis was related to a relative up-regulation of Bcl-2 consecutively followed by a delayed decrease in apoptosis activity.Conclusions/SignificanceIn the light of these results, we propose a model of heat stress in coral hosts whereby increasing temperatures engage activation of caspase 3-dependent apoptosis in cells designated for termination, but also the onset of a delayed protective response involving overexpression of Bcl-2 in surviving cells. This mitigating response to thermal stress could conceivably be an important regulatory mechanism for cell survival in corals exposed to sudden environmental changes.

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

“…Hence, if the caspase cascade is arrested at an early stage, the apoptotic response does not occur. Moreover, this response may be controlled by the balance between pro-and antiapoptotic molecules, such as the Bcl-2 and Bax gene families (19,24,40). The exact biochemical sequence triggering the caspase cascade in the host remains elusive; however, based on studies in metazoan models (41), we suggest that the ROS produced by the algal symbionts compromise the structural integrity of mitochondrial membrane in the host cells, thereby stimulating the release of factors initiating a caspase cascade.…”

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

“…2 reveals the first images of an isolated coral cell undergoing cytokine-induced apoptosis (42). We hypothesize that HuTNFα binds to one of the AdTNF receptors containing a death domain (AdTNF1-AdTNF6), initiating the apoptotic cascade and caspase activation (Fig.…”

“…In this study, we induced both of these cellular processes through the application of a single protein to adult coral tissue and individual coral cells. Although previous work has investigated the downstream effectors of apoptosis such as caspases (43) and Bcl-2 family members (42), this is the first examination, to our knowledge, of the upstream ligands and receptors involved with initiating apoptosis in coral. Recently published transcriptomic studies of corals exposed to various environmental stressors have implicated members of the TNFSF/TNFRSF, as well as downstream proteins involved with apoptosis, supporting the ecological relevance of the TNF pathway in coral (45)(46)(47)(48)(49).…”

Differential nitric oxide synthesis and host apoptotic events correlate with bleaching susceptibility in reef corals

“…Apoptosis is a highly conserved mechanism of programmed cell death (Kerr et al 1972) that is regulated by caspase enzymes (Lasi et al 2010). It is an important mechanism of symbiont loss during coral bleaching (Dunn et al 2004;Weis 2008;Pernice et al 2011) and is also a pathogen-removal strategy in metazoans (Carmen and Sinai 2007). The modification of apoptotic pathways has already been proposed as a mechanism for differential host cell survival post-bleaching (Tchernov et al 2011), and the anemone A. pallida generates NO to differing degrees during heat stress depending on the dominant in hospite symbiont genotype (Perez 2007).…”

“…Thus, the species selected for this study were chosen on the basis of their sensitivities to elevated temperature. We hypothesised that heating would result in the elevated synthesis of NO in host and symbiont and that host NO synthesis would correlate with the induction of apoptotic-like cell death pathways known to be involved in bleaching (Dunn et al 2004;Pernice et al 2011;Tchernov et al 2011). We also hypothesised that these events (in the host) are consequences of symbiont photophysiological dysfunction (Perez and Weis 2006).…”