Stress and death of cnidarian host cells play a role in cnidarian bleaching

Paxton, Camille W.; Davy, Simon K.; Weis, Virginia M.

doi:10.1242/jeb.087858

Cited by 56 publications

(77 citation statements)

References 38 publications

(46 reference statements)

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“…Further work is needed to fill in these gaps in our knowledge. While we cannot entirely discount symbiont-derived ROS as a stimulus for the host responses observed here, our data support a growing body of work suggesting that host-level mechanisms play an important role in determining the bleaching responses of corals (Nii and Muscatine 1997;Fitt et al 2009;Palmer et al 2010;Dunn et al 2012;Paxton et al 2013;Tolleter et al 2013). …”

Section: Cellular Events In the Coral Hostsupporting

confidence: 71%

“…Overproduction of reactive oxygen species (ROS), the onset of oxidative stress, and subsequent cellular damage were proposed as the proximate causes of this symbiotic collapse (Downs et al 2002). Temperature-and light-induced ROS generation have been experimentally confirmed in Symbiodinium (Lesser 1996;Lesser 2006 for review;Suggett et al 2008;Saragosti et al 2010), but damage to host tissue in the absence of symbiont dysfunction (Gates et al 1992;Nii and Muscatine 1997;Dunn et al 2004Dunn et al , 2012Paxton et al 2013) and the release of photosynthetically competent and viable symbionts from bleaching corals (Ralph et al 2001;Hill and Ralph 2007) have also been reported. Clearly, not all thermal bleaching in corals is symbiontdriven (Baird et al 2008;Tolleter et al 2013).…”

Section: Communicated By Biology Editor Dr Anastazia Banaszakmentioning

confidence: 99%

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

et al. 2014

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Coral bleaching poses a threat to coral reefs worldwide. As a consequence of the temperature-induced breakdown in coral-dinoflagellate symbiosis, bleaching can have extensive effects on reef communities. However, our understanding of bleaching at a cellular level is limited, and this is particularly true regarding differential susceptibility among coral species. Recent work suggests that bleaching may represent a host innate immune-like response to symbiont dysfunction that involves synthesis of the signalling compound nitric oxide (NO) and the induction of host apoptotic-like cell death. In this study, we examined the activity of apoptosis-regulating enzymes alongside oxidised NO accumulation (a proxy for NO synthesis) in the reef corals Acropora millepora, Montipora digitata, and Pocillopora damicornis during experimental thermal stress. P. damicornis was the most sensitive species, suffering mortality (tissue sloughing) after 5 days at 33°C but non-lethal bleaching after 9 days at 31.5°C. A. millepora bleached at 33°C but remained structurally intact, while M. digitata showed little evidence of bleaching. P. damicornis and A. millepora both exhibited evidence of temperature-induced NO synthesis and, after 5 days of heating, levels of oxidised NO in both species were fivefold higher than in controls maintained at 28.5°C. These responses preceded bleaching by a number of days and may have occurred before symbiont dysfunction (measured as chlorophyll a degradation and oxidised NO accumulation). In A. millepora, apparent NO synthesis correlated with the induction of host apoptotic-like pathways, while in P. damicornis, the upregulation of apoptotic pathways occurred later. No evidence of elevated NO production or apoptosis was observed in M. digitata at 33°C and baseline activity of apoptosis-regulating enzymes was negligible in this species. These findings provide important physiological data in the context of the responses of corals to global change and suggest that early events in the host may be important in the collapse of the coral-dinoflagellate symbiosis.

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Section: Cellular Events In the Coral Hostsupporting

confidence: 71%

Section: Communicated By Biology Editor Dr Anastazia Banaszakmentioning

confidence: 99%

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

et al. 2014

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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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“…Moreover, while some intracellular sites and effects of thermal damage in the host and symbiont have been identified, there is no consensus about the causal chain of events and the supposed 'weak link' in the symbiosis. Indeed, bleaching can be manifested as host-cell detachment and/or release of potentially photosynthetically competent symbionts (Gates et al, 1992;Ralph et al, 2001), as well as breakdown of photosynthetic dark and light reactions (Jones et al, 1998;Warner et al, 1999), and apoptosis and necrosis in both partners (Dunn et al, 2004;Tchernov et al, 2011;Hawkins et al, 2013;Paxton et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

Differential coral bleaching—Contrasting the activity and response of enzymatic antioxidants in symbiotic partners under thermal stress

Krueger

Hawkins

Becker

et al. 2015

Comparative Biochemistry and Physiology Part A: Molecular &

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118

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Mass coral bleaching due to thermal stress represents a major threat to the integrity and functioning of coral reefs. Thermal thresholds vary, however, between corals, partly as a result of the specific type of endosymbiotic dinoflagellate (Symbiodinium sp.) they harbour. The production of reactive oxygen species (ROS) in corals under thermal and light stress has been recognised as one mechanism that can lead to cellular damage and the loss of their symbiont population (Oxidative Theory of Coral Bleaching). Here, we compared the response of symbiont and host enzymatic antioxidants in the coral species Acropora millepora and Montipora digitata at 28°C and 33°C. A. millepora at 33°C showed a decrease in photochemical efficiency of photosystem II (PSII) and increase in maximum midday excitation pressure on PSII, with subsequent bleaching (declining photosynthetic pigment and symbiont density). M. digitata exhibited no bleaching response and photochemical changes in its symbionts were minor. The symbiont antioxidant enzymes superoxide dismutase, ascorbate peroxidase, and catalase peroxidase showed no significant upregulation to elevated temperatures in either coral, while only catalase was significantly elevated in both coral hosts at 33°C. Increased host catalase activity in the susceptible coral after 5 days at 33°C was independent of antioxidant responses in the symbiont and preceded significant declines in PSII photochemical efficiencies. This finding suggests a potential decoupling of host redox mechanisms from symbiont photophysiology and raises questions about the importance of symbiont-derived ROS in initiating coral bleaching.

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Stress and death of cnidarian host cells play a role in cnidarian bleaching

Cited by 56 publications

References 38 publications

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

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

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

Differential coral bleaching—Contrasting the activity and response of enzymatic antioxidants in symbiotic partners under thermal stress

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