Symbiosis-induced adaptation to oxidative stress

Abstract

Cnidarians in symbiosis with photosynthetic protists must withstand daily hyperoxic/anoxic transitions within their host cells. Comparative studies between symbiotic (Anemonia viridis) and non-symbiotic (Actinia schmidti) sea anemones show striking differences in their response to oxidative stress. First, the basal expression of SOD is very different. Symbiotic animal cells have a higher isoform diversity (number and classes) and a higher activity than the non-symbiotic cells. Second, the symbiotic animal cells of A. viridis also maintain unaltered basal values for cellular damage when exposed to experimental hyperoxia (100%·O 2 ) or to experimental thermal stress (elevated temperature +7°C above ambient). Under such conditions, A. schmidti modifies its SOD activity significantly. Electrophoretic patterns diversify, global activities diminish and cell damage biomarkers increase. These data suggest symbiotic cells adapt to stress while non-symbiotic cells remain acutely sensitive. In addition to being toxic, high O 2 partial pressure (P O ∑) may also constitute a preconditioning step for symbiotic animal cells, leading to an adaptation to the hyperoxic condition and, thus, to oxidative stress. Furthermore, in aposymbiotic animal cells of A. viridis, repression of some animal SOD isoforms is observed. Meanwhile, in cultured symbionts, new activity bands are induced, suggesting that the host might protect its zooxanthellae in hospite. Similar results have been observed in other symbiotic organisms, such as the sea anemone Aiptasia pulchella and the scleractinian coral Stylophora pistillata. Molecular or physical interactions between the two symbiotic partners may explain such variations in SOD activity and might confer oxidative stress tolerance to the animal host.

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

“…the applied heating rate in the experimental setup. Low heating rates profoundly delay the physiological response of the coral holobiont (Middlebrook et al, 2010) and the ramping rate of 1°C day -1 used in the current study is considerably slower than in previous studies of antioxidant responses under thermal stress; these applied heating rates ranging from near-instantaneous to 4°C hour -1 (Yakovleva et al, 2004;Richier et al, 2005;Higuchi et al, 2008;Yakovleva et al, 2009;Higuchi et al, 2012;Downs et al, 2013;T. Higuchi and I. Yakovleva, personal communication).…”

“…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. 1; Nii and Muscatine, 1997;Richier et al, 2005). The presence of a high hydrogen peroxide concentration of host origin could also explain the KatG increase and APX inhibition in the symbionts of A. millepora on the final day of observation, since neither was related to changes in symbiont SOD levels.…”

“…With regard to the role of light and temperature in inducing oxidative stress in both compartments of the cnidarian-dinoflagellate symbiosis, previous findings are ambiguous. While temperature stress increased symbiont SOD activity in Anemonia viridis (Richier et al, 2005) and Galaxea fascicularis (Higuchi et al, 2008;Higuchi et al, 2012), consistent with photophysiological stress and the formation of superoxide via the Mehler reaction (Asada, 1984), host SOD may (Montastraea faveolata; Downs et al, 2000; Stylophora pistillata; Yakovleva et al, 2004) or may not (Platygyra ryukyuensis; Yakovleva et al, 2004;Anemonia viridis;Richier et al, 2005) respond to elevated temperature. Similarly, increased host tissue levels of ROS, in the form of superoxide or hydroxyl radicals in response to elevated temperature can be either present (Aiptasia pulchella; Nii and Muscatine, 1997) or absent (Galaxea fascicularis; Higuchi et al, 2010).…”

Symbiosis-dependent gene expression in coral–dinoflagellate association: cloning and characterization of a P-type H+-ATPase gene

“…However, these genes are not symbiosis-specific since they are also expressed, at a lower level, in aposymbiotic animals. In the same manner, Richier et al (2005) have shown an increased superoxide dismutase (SOD) activity in symbiotic anemones compared with aposymbiotic. At a genetic level, six expressed sequence tags (ESTs) and 91 host unigenes that are differentially expressed in symbiotic state have been characterized so far (Rodriguez-Lanetty et al 2006;deBoer et al 2007).…”

Increased susceptibility of algal symbionts to photo-inhibition resulting from the perturbation of coral gastrodermal membrane trafficking

“…However, it was found that light irradiation reduced BODIPY-SM degradation (Table 1), which should result from an alteration in membrane trafficking of the host plasma membrane along a lysosome-like pathway. Free-radical species such as ROS are generated during the light reactions of photosynthesis [39]. The use of fluorescent probes indicated that ROS were not produced at substantial levels until 3 h of light irradiation had occurred, the time at which noticeable membrane perturbation, as evidenced by labeling with Calcofluor White M2R, was observed ( Figure 3).…”