Nitric Oxide and Cnidarian-Dinoflagellate Symbioses: Pieces of a Puzzle

Trapido-Rosenthal, Henry G.; Sharp, Katherine H.; Galloway, Tamara S.; Morrall, Clare E.

doi:10.1093/icb/41.2.247

Cited by 21 publications

(31 citation statements)

References 50 publications

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“…Since peroxynitrite is very reactive under physiological conditions and formed by the reaction between nitric oxide (NO•) and O 2 •− , the presence of high concentrations of GFP in corals would not only be useful in preventing the formation of hydroxyl radicals but also in preventing the formation of peroxynitrite since NO• is known to occur in symbiotic cnidarians and nitric oxide synthase activity increases in corals experiencing thermal stress [35,36].…”

Section: Discussionmentioning

confidence: 99%

Quenching of superoxide radicals by green fluorescent protein

Bou-Abdallah

Chasteen

Lesser

2006

Biochimica et Biophysica Acta (BBA) - General Subjects

162

144

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Green fluorescent protein (GFP) is a widely used in vivo molecular marker. These proteins are particularly resistant, and maintain function, under a variety of cellular conditions such as pH extremes and elevated temperatures. Green fluorescent proteins are also abundant in several groups of marine invertebrates including reef-forming corals. While molecular oxygen is required for the post-translational maturation of the protein, mature GFPs are found in corals where hyperoxia and reactive oxygen species (ROS) occur due to the photosynthetic activity of algal symbionts. In vitro spin trapping electron paramagnetic resonance and spectrophotometric assays of superoxide dismutase (SOD)-like enzyme activity show that wild type GFP from the hydromedusa, Aequorea victoria, quenches superoxide radicals (O 2 •− ) and exhibits SOD-like activity by competing with cytochrome c for reaction with O 2 •− . When exposed to high amounts of O 2 •− the SOD-like activity and protein structure of GFP are altered without significant changes to the fluorescent properties of the protein. Because of the distribution of fluorescent proteins in both the epithelial and gastrodermal cells of reef-forming corals we propose that GFP, and possibly other fluorescent proteins, can provide supplementary antioxidant protection.

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Section: Discussionmentioning

confidence: 99%

Quenching of superoxide radicals by green fluorescent protein

Bou-Abdallah

Chasteen

Lesser

2006

Biochimica et Biophysica Acta (BBA) - General Subjects

162

144

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“…This is a common innate immune pathway observed in other animals, which leads to downstream elimination of invading microbes by various mechanisms including host programmed cell death or apoptosis (Kumar et al, 2004;Pacher et al, 2007). However, two other studies found high concentrations of NO in cultured or freshly isolated symbionts with elevated temperature (Bouchard and Yamasaki, 2008;Trapido-Rosenthal et al, 2001). This provides evidence that NO is a direct signaling molecule between the partners of symbiosis that could initiate a bleaching cascade.…”

Section: Ros Concentration and Production In Host Tissuesmentioning

confidence: 99%

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

Weis

2008

Journal of Experimental Biology

808

980

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SummaryCnidarian bleaching is a breakdown in the mutualistic symbiosis between host Cnidarians, such as reef building corals, and their unicellular photosynthetic dinoflagellate symbionts. Bleaching is caused by a variety of environmental stressors, most notably elevated temperatures associated with global climate change in conjunction with high solar radiation, and it is a major contributor to coral death and reef degradation. This review examines the underlying cellular events that lead to symbiosis dysfunction and cause bleaching, emphasizing that, to date, we have only some pieces of a complex cellular jigsaw puzzle. Reactive oxygen species (ROS), generated by damage to both photosynthetic and mitochondrial membranes, is shown to play a central role in both injury to the partners and to inter-partner communication of a stress response. Evidence is presented that suggests that bleaching is a host innate immune response to a compromised symbiont, much like innate immune responses in other host-microbe interactions. Finally, the elimination or exit of the symbiont from host tissues is described through a variety of mechanisms including exocytosis, host cell detachment and host cell apoptosis.

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“…The synthesis of NO, an antimicrobial and cell-signalling molecule (Wink and Mitchell 1998;Fang 2004;Wang and Ruby 2011), has been reported in symbiotic cnidarians (Perez and Weis 2006) and dinoflagellates (Trapido-Rosenthal et al 2001;Bouchard and Yamasaki 2008;Hawkins and Davy 2012). In the host, NO generation during temperature stress is thought to form part of an innate immune-like response mediating the ejection of Symbiodinium cells from the symbiosis (Perez and Weis 2006;Weis 2008;Detournay and Weis 2011;Detournay et al 2012).…”

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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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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Nitric Oxide and Cnidarian-Dinoflagellate Symbioses: Pieces of a Puzzle

Cited by 21 publications

References 50 publications

Quenching of superoxide radicals by green fluorescent protein

Quenching of superoxide radicals by green fluorescent protein

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

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

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