Abstract

Marine Synechococcus undergo a wide range of environmental stressors, especially high and variable irradiance, which may induce oxidative stress through the generation of reactive oxygen species (ROS). While light and ROS could act synergistically on the impairment of photosynthesis, inducing photodamage and inhibiting photosystem II repair, acclimation to high irradiance is also thought to confer resistance to other stressors. To identify the respective roles of light and ROS in the photoinhibition process and detect a possible light-driven tolerance to oxidative stress, we compared the photophysiological and transcriptomic responses of Synechococcus sp. WH7803 acclimated to low light (LL) or high light (HL) to oxidative stress, induced by hydrogen peroxide (H₂O₂) or methylviologen. While photosynthetic activity was much more affected in HL than in LL cells, only HL cells were able to recover growth and photosynthesis after the addition of 25 μM H₂O₂. Depending upon light conditions and H₂O₂ concentration, the latter oxidizing agent induced photosystem II inactivation through both direct damage to the reaction centers and inhibition of its repair cycle. Although the global transcriptome response appeared similar in LL and HL cells, some processes were specifically induced in HL cells that seemingly helped them withstand oxidative stress, including enhancement of photoprotection and ROS detoxification, repair of ROS-driven damage, and regulation of redox state. Detection of putative LexA binding sites allowed the identification of the putative LexA regulon, which was down-regulated in HL compared with LL cells but up-regulated by oxidative stress under both growth irradiances.

Highlights

  • Marine Synechococcus undergo a wide range of environmental stressors, especially high and variable irradiance, which may induce oxidative stress through the generation of reactive oxygen species (ROS)

  • The physiological experiments performed in this study revealed that under their growth irradiance, high light (HL)-acclimated cells were more affected than low light (LL) cells by H2O2 stress with regard to PSII photoinactivation, and this was verified across the whole range of H2O2 concentrations tested (Figs. 1 and 2)

  • By testing a range of oxidant concentrations and treatment durations on LL and HL cultures, we show that, depending upon the oxidant concentration, PSII damage observed in oxidant-stressed HL cells results both from cumulative effects of direct ROS damage to PSII and ROS inhibition of the rapid PSII repair needed to counter the high photoinactivation rate

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Summary

Introduction

Marine Synechococcus undergo a wide range of environmental stressors, especially high and variable irradiance, which may induce oxidative stress through the generation of reactive oxygen species (ROS). While light and ROS could act synergistically on the impairment of photosynthesis, inducing photodamage and inhibiting photosystem II repair, acclimation to high irradiance is thought to confer resistance to other stressors. To identify the respective roles of light and ROS in the photoinhibition process and detect a possible light-driven tolerance to oxidative stress, we compared the photophysiological and transcriptomic responses of Synechococcus sp. The global transcriptome response appeared similar in LL and HL cells, some processes were induced in HL cells that seemingly helped them withstand oxidative stress, including enhancement of photoprotection and ROS detoxification, repair of ROS-driven damage, and regulation of redox state. At the PSII results in the formation of H2O2 donor side, incomplete oxidation of water at the water-splitting manganese complex iornexddiduuicczeeedsdtihninetotofoOOrHm2··-abtbiyyofnmreoeafnmHgea2tnOael2ss, ewrechloeimachspeldceaxbnyrbadedaifmcuaraltsgheoedrr

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