Cellular mechanisms of Cnidarian bleaching: stress causes the collapse of symbiosis

Weis, Virginia M.

doi:10.1242/jeb.009597

Cited by 789 publications

(1,050 citation statements)

References 66 publications

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“…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. In the case of sensitive corals, it is most likely that ROS levels will continue to accumulate after bleaching as a result of mitochondrial dysfunction and further evoke the apoptotic machinery (6,33,42).…”

Section: Discussionmentioning

confidence: 99%

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

Tchernov

Kvitt

Haramaty

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

183

182

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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.

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Section: Discussionmentioning

confidence: 99%

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

Tchernov

Kvitt

Haramaty

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

183

182

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“…The studies suggested that host cell death can contribute to subsequent symbiont cell mortality, a process that appears similar to a host innate immune response. The results indicated that no single pathway is responsible for symbiont release during bleaching, allowing to formulate a model for cellular processes involved in the control of cnidarian bleaching where apoptosis and autophagy act together in a see-saw mechanism such that if one is inhibited the other is induced (Dunn et al 2007;Weis 2008;Paxton et al 2013).…”

Section: Autophagy Induced By Environmental Stress On Aquatic Invertementioning

confidence: 99%

Autophagy as a defense strategy against stress: focus on Paracentrotus lividus sea urchin embryos exposed to cadmium

Chiarelli

Martino

Agnello

et al. 2016

Cell Stress and Chaperones

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Autophagy is used by organisms as a defense strategy to face environmental stress. This mechanism has been described as one of the most important intracellular pathways responsible for the degradation and recycling of proteins and organelles. It can act as a cell survival mechanism if the cellular damage is not too extensive or as a cell death mechanism if the damage/stress is irreversible; in the latter case, it can operate as an independent pathway or together with the apoptotic one. In this review, we discuss the autophagic process activated in several aquatic organisms exposed to different types of environmental stressors, focusing on the sea urchin embryo, a suitable system recently included into the guidelines for the use and interpretation of assays to monitor autophagy. After cadmium (Cd) exposure, a heavy metal recognized as an environmental toxicant, the sea urchin embryo is able to adopt different defense mechanisms, in a hierarchical way. Among these, autophagy is one of the main responses activated to preserve the developmental program. Finally, we discuss the interplay between autophagy and apoptosis in the sea urchin embryo, a temporal and functional choice that depends on the intensity of stress conditions.

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“…In corals, apoptosis has been observed in response to hyperthermic oxidative stress, disease, and as a postphagocytic removal mechanism of zooxanthellae during the onset of symbiosis (10,12). The recent Acropora digitfera genome suggests that coral possess homologs to the human intrinsic and extrinsic apoptotic pathways (13).…”

Section: Significancementioning

confidence: 99%

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

Quistad

Stotland

Barott

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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The Precambrian explosion led to the rapid appearance of most major animal phyla alive today. It has been argued that the complexity of life has steadily increased since that event. Here we challenge this hypothesis through the characterization of apoptosis in reef-building corals, representatives of some of the earliest animals. Bioinformatic analysis reveals that all of the major components of the death receptor pathway are present in coral with high-predicted structural conservation with Homo sapiens. The TNF receptor-ligand superfamilies (TNFRSF/TNFSF) are central mediators of the death receptor pathway, and the predicted proteome of Acropora digitifera contains more putative coral TNFRSF members than any organism described thus far, including humans. This high abundance of TNFRSF members, as well as the predicted structural conservation of other death receptor signaling proteins, led us to wonder what would happen if corals were exposed to a member of the human TNFSF (HuTNFα). HuTNFα was found to bind directly to coral cells, increase caspase activity, cause apoptotic blebbing and cell death, and finally induce coral bleaching. Next, immortalized human T cells (Jurkats) expressing a functional death receptor pathway (WT) and a corresponding Fas-associated death domain protein (FADD) KO cell line were exposed to a coral TNFSF member (AdTNF1) identified and purified here. AdTNF1 treatment resulted in significantly higher cell death (P < 0.0001) in WT Jurkats compared with the corresponding FADD KO, demonstrating that coral AdTNF1 activates the H. sapiens death receptor pathway. Taken together, these data show remarkable conservation of the TNF-induced apoptotic response representing 550 My of functional conservation. evolution immunity | cytokines | Cnidarians | climate change | invertebrate immunity

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Cellular mechanisms of Cnidarian bleaching: stress causes the collapse of symbiosis

Cited by 789 publications

References 66 publications

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

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

Autophagy as a defense strategy against stress: focus on Paracentrotus lividus sea urchin embryos exposed to cadmium

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

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