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Imbalance between oxygen photoreduction and antioxidant capacities in Symbiodinium cells exposed to combined heat and high light stress

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Abstract

During the last decades, coral reefs have been affected by several large-scale bleaching events, and such phenomena are expected to increase in frequency and severity in the future, thus compromising their survival. High sea surface temperature accompanied by high levels of solar irradiance has been found to be responsible for the induction of oxidative stress ultimately ending with the disruption of the symbiosis between cnidarians and Symbiodinium. For two decades, many studies have pointed to the water–water cycle (WWC) as being one of the primary mediators of this phenomenon, but the impacts of environmental stress on the O2 reduction by PSI and the associated reactive oxygen species (ROS)-detoxifying enzymes remain to be determined. In this study, we analyzed the impacts of acute thermal and light stress on the WWC in the model Symbiodinium strain A1. We observed that the high light treatment at 26 °C resulted in the up-regulation of superoxide dismutase, ascorbate peroxidase, and glutathione reductase activities and an increased production of ROS with no significant change in O2-dependent electron transport. Under high light and at 33 °C, O2-dependent electron transport was significantly increased relative to total electron transport. This increase was concomitant with a twofold increase in ROS generation compared with the treatment at 26 °C, while enzymes involved in the WWC were largely inactivated. These data show for the first time that combined heat and light stress inactivate antioxidant capacities of the WWC and suggests that its photoprotective functions are overwhelmed under these conditions. This study also indicates that cnidarians may be more prone to bleach if they harbor Symbiodinium cells having a highly active Mehler-type electron transport, unless they are able to quickly up-regulate their antioxidant capacities.

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Acknowledgments

This work was supported by grants from the Fonds National de la Recherche Scientifique (FRFC 2.4.631.09 and FRFC. 2.4597, CDR J.0032.1, and MIS F.4520 to PC) and from the University of Liège (C-13/22 to JCP and FF). PC and FF are Research Associate and Research Director from FRS-FNRS. We thank Dr P. Meyer for advices on statistical analysis and the two anonymous reviewers for their comments.

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  1. Ecophysiologie et Physiologie Animale, Département de Biologie, Ecologie et Evolution, Université de Liège, 27 Bld du rectorat, 4000, Liège, Belgium

    S. Roberty, D. Fransolet & J.-C. Plumier

  2. Laboratoire de Génétique et Physiologie des Microalgues, Phytosystems, Département des Sciences de la vie, Université de Liège, 27 Bld du rectorat, 4000, Liège, Belgium

    P. Cardol

  3. Laboratoire de Bioénergétique, Phytosystems, Département des Sciences de la vie, Université de Liège, 27 Bld du rectorat, 4000, Liège, Belgium

    F. Franck

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  1. S. Roberty
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  2. D. Fransolet
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Roberty, S., Fransolet, D., Cardol, P. et al. Imbalance between oxygen photoreduction and antioxidant capacities in Symbiodinium cells exposed to combined heat and high light stress. Coral Reefs 34, 1063–1073 (2015). https://doi.org/10.1007/s00338-015-1328-5

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