Nitric oxide and cnidarian bleaching: an eviction notice mediates breakdown of a symbiosis

Abstract

presented here show that the host cell is a major source of NO during exposure to elevated temperatures and that this constitutes a cytotoxic response leading to bleaching. These results have important evolutionary implications as the observed NO production in these basal metazoans displays many parallels to the cytotoxic inflammatory response to pathogens, a well-understood process in mammalian model systems.

Hyperthermic stress-induced increase in the expression of glutamate-cysteine ligase and glutathione levels in the symbiotic sea anemone Aiptasia pallida

“…Nevertheless, both oxidative or nitrosative stress may increase the formation of PSSG (Dalle-Donne et al, 2007). Strikingly, Perez and Weis (2006) have shown that nitric oxide (NO) is generated during hyperthermal stress exposure in A. pallida, while NO has been proposed as an intracellular regulator of PSSG formation (West et al, 2006). Based on this, we hypothesize that NOmediated S-glutathionylation of specific target proteins is a regulatory mechanism during the process of cnidarian bleaching.…”

“…2). Earlier studies have documented that heat-stress evokes oxidative and nitrosative stress in symbiotic anemones (Dunn et al, 2002;Perez and Weis 2006;Richier et al, 2006); thus, the increase in GCLC gene expression is likely to reflect the increased demand of intracellular GSH as an adaptive response. The increase in total GSH amounts could be due to a number of reasons, all of which may play important roles during the process of cnidarian bleaching.…”

“…Experimental studies have demonstrated that the hyperthermic stress-induced loss of symbiotic algae in the sea anemone Aiptasia pallida is associated with nitric oxide generation (Perez et al, 2001 ;Perez and Weis, 2006). These results strongly suggest a role of free radicals as a signaling interface between exposure to hyperthermic stress and a cellular response.…”

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

“…Symbiodinium cells are located within arrested phagosomes and a breakdown of hostsymbiont recognition mechanisms under stress might lead to their maturation to phagolysosomes. Antipathogenic responses in mature phagolysosomes involve the generation of ROS and nitric oxide (Wink et al, 2011) and thermal stress-induced production of nitric oxide in symbiotic cnidarians has been associated with the apoptotic-like cell death pathways, that themselves are significant cellular mechanisms of bleaching (Perez and Weis, 2006;Dunn and Weis, 2009;Hawkins et al, 2013). The potential importance of host-produced hydrogen peroxide is highlighted in the current study, where host catalase activity in A. millepora at 33°C remained high until the end of the experiment, despite photosynthetic breakdown (and loss of pigment) that might be expected to limit ROS synthesis as a result of lower rates of oxygen evolution and tissue pO2 in advanced bleaching states ( Fig.…”

“…In addition, high levels of ROS as well as reactive nitrogen species (RNS) in the host gastrodermal cell could stimulate innate immune-like pathways and potentially trigger pro-apoptotic processes in the host (Fig. 1, Perez and Weis, 2006;Dunn et al, 2007;Hawkins et al, 2013). The involvement of ROS in coral bleaching led to the proposal of a unifying mechanistic model of coral bleaching: the 'Oxidative Theory of Coral Bleaching' (OTB).…”