Pairing Up Pays Off: Symbiosis confers tolerance to environmental stresses.

A review of: Richier S et al (2004) Symbiosis-induced adaptation to oxidative stress. Journal of Experimental Biology, 208: 277-285. France.

O₂ has low toxicity but can be converted to more toxic reactive oxygen species (ROS) such as superoxide during hyperoxia. Diurnal variations in O₂ levels in tissues are well documented in photosynthetic organisms such as plants and symbiotic cnidarians.

Superoxide dismutase (SOD) is the first line of anti-oxidant defence from ROS in aerobic organisms. This enzyme is highly conserved across kingdoms and is observed even when other enzymes (i.e. catalase, which works in conjunction with SOD) are not present. Plants are known to contain between 4-8 isoforms of SOD while animals have 2-3. The authors have previously described (Richier et al 2003) a large diversity of SOD isoforms from 3 well known SOD classes (Mn, CuZn and FeSOD) in symbiotic Anemonia viridis and Stylophora pistillata. A MnSOD (typically found in the mitochondria) in A. viridis tissues was also observed outside the mitochondria, along with an FeSOD isoform typical in CO₂ fixing organisms but not in animals.

The aim of the study was to determine the role of symbiosis in oxidative stress and thermal tolerance, as well as to assess the role of the symbiont in expression of specific SOD isoforms in animal cells. Richier et al (2004) compared effects of hyperoxia between two sea anemones, symbiotic A. viridis and non-symbiotic Actinia schmidti. Biomarkers such as protein carbonylation as a measure of protein oxidation and malondialdehyde as a measure of lipid peroxidation were used to gauge cellular damage. SOD activity was used as a biomarker for anti-oxidant defence.

Native gel electrophoresis identified five activity bands from Mn, CuZn and FeSOD in A. viridis and three bands from two isoforms of CuZnSOD, with one MnSOD in A. schmidti controls. Moreover, quantitative analysis revealed 1.8x higher SOD activity in A. viridis (10.5 U mg^-1) when compared to A. schmidti (5.88 U mg^-1). After 10 hours of exposure to hyperoxia, there was no change in SOD isoform expression in A. viridis but a new isoform of CuZnSOD and a slight decrease in SOD activity was observed in A. schmidti. In addition, there was no significant variation in damage biomarkers in the symbiotic anemone, in contrast to a six-fold increase in protein carbonylation seen in the non-symbiotic anemone. After 5 days of elevated water temperature a three-fold increase in protein oxidation was observed in A. viridis, but a ten-fold increase in protein oxidation and a three-fold increase in lipid peroxidation was detected in A. schmidti.

The effects of elevated temperature on symbiotic and aposymbiotic (bleached) specimens were described using anemones A. viridis and Aiptasia pulchella. Bleached A. viridis and A. pulchella exhibited an overall decrease in SOD activity in both endoderm and ectoderm, with the loss of some activity bands from Mn and FeSOD in A. viridis and the loss of 3 MnSOD isoforms in A. pulchella.

Diversity of SOD isoforms in animal cells living with photosynthetic dinoflagellates is associated with increase in overall SOD activity, as a consequence of host adaptation to symbiont photosynthesis and elevated ROS production during exposure to light. The sensitivity of non-symbiotic A. schmidti to elevated oxygen and temperature suggests symbiosis is crucial in conferring host cell adaptations to environmental stresses, such as enhanced antioxidant defences, to limit and/or avoid cellular damage.

The decrease in SOD activity in aposymbiotic specimen tissues in both endoderm and ectoderm (which doesn’t have zooxanthellae) suggests a decrease in oxidative stress in response to a decrease in photosynthetic activity, and possibly as a result of disruption of the anthozoans’ normal cellular processes.

The possibly cytosolic MnSOD and FeSOD described by Richier et al (2003) in animal tissues is rather unusual and could be an evolutionary adaptation to hypoxia. It is also possible that genes were exchanged between the two closely associated organisms. What is evident is hyperoxia induced by symbiont photosynthesis necessitates higher antioxidant defences in the host. Moreover, the hyperoxic adaptation of the symbiotic species may also be a preconditioning step to limit cellular damage by various environmental factors, such as elevated water temperature. There is clearly a complex interplay between host cells and symbionts which is to be the subject for further investigation.

Additional Reference:

Richier S et al (2003) Characterization of superoxide dismutases in anoxia- and hyperoxia-tolerant symbiotic cnidarians. Biochimica et Biophysica Acta, 1621: 84-91. France.