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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.

SUBMITTER: Tchernov D

PROVIDER: S-EPMC3116386 | biostudies-other | 2011 Jun

REPOSITORIES: biostudies-other

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

Tchernov Dan D Kvitt Hagit H Haramaty Liti L Bibby Thomas S TS Gorbunov Maxim Y MY Rosenfeld Hanna H Falkowski Paul G PG

Proceedings of the National Academy of Sciences of the United States of America 20110602 24

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 ...[more]

PMID: 21636790

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Project description:BackgroundCoral bleaching can be defined as the loss of symbiotic zooxanthellae and/or their photosynthetic pigments from their cnidarian host. This major disturbance of reef ecosystems is principally induced by increases in water temperature. Since the beginning of the 1980s and the onset of global climate change, this phenomenon has been occurring at increasing rates and scales, and with increasing severity. Several studies have been undertaken in the last few years to better understand the cellular and molecular mechanisms of coral bleaching but the jigsaw puzzle is far from being complete, especially concerning the early events leading to symbiosis breakdown. The aim of the present study was to find molecular actors involved early in the mechanism leading to symbiosis collapse.ResultsIn our experimental procedure, one set of Pocillopora damicornis nubbins was subjected to a gradual increase of water temperature from 28 degrees C to 32 degrees C over 15 days. A second control set kept at constant temperature (28 degrees C). The differentially expressed mRNA between the stressed states (sampled just before the onset of bleaching) and the non stressed states (control) were isolated by Suppression Subtractive Hybridization. Transcription rates of the most interesting genes (considering their putative function) were quantified by Q-RT-PCR, which revealed a significant decrease in transcription of two candidates six days before bleaching. RACE-PCR experiments showed that one of them (PdC-Lectin) contained a C-Type-Lectin domain specific for mannose. Immunolocalisation demonstrated that this host gene mediates molecular interactions between the host and the symbionts suggesting a putative role in zooxanthellae acquisition and/or sequestration. The second gene corresponds to a gene putatively involved in calcification processes (Pdcyst-rich). Its down-regulation could reflect a trade-off mechanism leading to the arrest of the mineralization process under stress.ConclusionUnder thermal stress zooxanthellae photosynthesis leads to intense oxidative stress in the two partners. This endogenous stress can lead to the perception of the symbiont as a toxic partner for the host. Consequently, we propose that the bleaching process is due in part to a decrease in zooxanthellae acquisition and/or sequestration. In addition to a new hypothesis in coral bleaching mechanisms, this study provides promising biomarkers for monitoring coral health.

Project description:In 2016, global temperatures were the highest on record, and mass coral bleaching occurred world-wide. However, around Sesoko Island, Okinawa, southwestern Japan, the heat stress assessed by degree heating week (DHW) based on local temperature measurements was moderate in 2016; in 1998, DHW was three times higher than in 2016 (10.6 vs. 3.3 in September in respective years). On a reef flat of Sesoko Island where the effect of severe coral bleaching on coral assemblage was monitored in 1998, significant coral bleaching occurred in 2016. Bleaching of the heat stress sensitive Acropora corals began in July 2016 on the reef flat as seawater temperature rose. We observed the bleaching and post-bleaching mortality status of individual colonies of Acropora spp. in 2016 in fixed plots on the reef flat. In total, 123 Acropora colonies were followed for six months after seawater temperature became normal by multiple surveys. At the beginning of September 2016, 99.2% of colonies, were either completely (92.7%) or partially (6.5%) bleached. Of those, the dominant species or species groups were A. gemmifera (Ag), A. digitifera (Ad), and tabular Acropora (tA). For all Acropora colonies, the overall whole and partial mortality was 41.5% and 11.4%, respectively. Whole mortality rate differed significantly among species; 72.5%, 17.9%, and 27.8% in Ag, Ad, and tA, respectively. Mortality rates at the end of the surveys were similar in smaller (?10 cm in diameter) and larger Ag, but the former suffered mortality earlier than the latter. Higher survival of smaller colonies was observed only in tA (100%), which may be associated with large morphological differences between smaller and larger colonies. Some of the dominant Acropora colonies had survived without partial mortality including 15.0% survival of the most vulnerable Ag at the end of the surveys. These results suggest that moderate heat stress may have a potential for selecting heat-tolerant genotypes. A longer period of mortality lasting for six months, was observed in Ag in addition to immediate whole mortality after bleaching, due to the continuous loss of living tissue by partial mortality. This highlights the need for multiple surveys at least during several months to accurately assess the impact of thermal stress event to corals. In contrast to DHW based on local measurements, DHW obtained from satellite data were similar between 1998 and 2016. Although satellite-based measurement of sea surface temperature is very useful to reveal variations in heat stress at a large spatial scale, temperature should be measured on site when variations at smaller spatial scales are of interest.

Dataset Information

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

Publications

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

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