Light-independent regulation of algal photoprotection by CO2 availability

M. Águila Ruiz-Sola, Serena Flori, Yizhong Yuan, Gaelle Villain, Emanuel Sanz-Luque, Petra Redekop, Ryutaro Tokutsu, Anika Küken, Angeliki Tsichla, Georgios Kepesidis, Guillaume Allorent, Marius Arend, Fabrizio Iacono, Giovanni Finazzi, Michael Hippler, Zoran Nikoloski, Jun Minagawa, Arthur R. Grossman and Dimitris Petroutsos ()
Additional contact information
M. Águila Ruiz-Sola: Univ. Grenoble Alpes, CNRS, CEA, INRAE, IRIG-LPCV
Serena Flori: Univ. Grenoble Alpes, CNRS, CEA, INRAE, IRIG-LPCV
Yizhong Yuan: Univ. Grenoble Alpes, CNRS, CEA, INRAE, IRIG-LPCV
Gaelle Villain: Univ. Grenoble Alpes, CNRS, CEA, INRAE, IRIG-LPCV
Emanuel Sanz-Luque: The Carnegie Institution for Science, Department of Plant Biology
Petra Redekop: The Carnegie Institution for Science, Department of Plant Biology
Ryutaro Tokutsu: Division of Environmental photobiology, National Institute for Basic Biology (NIBB)
Anika Küken: University of Potsdam
Angeliki Tsichla: Univ. Grenoble Alpes, CNRS, CEA, INRAE, IRIG-LPCV
Georgios Kepesidis: Univ. Grenoble Alpes, CNRS, CEA, INRAE, IRIG-LPCV
Guillaume Allorent: Univ. Grenoble Alpes, CNRS, CEA, INRAE, IRIG-LPCV
Marius Arend: University of Potsdam
Fabrizio Iacono: Univ. Grenoble Alpes, CNRS, CEA, INRAE, IRIG-LPCV
Giovanni Finazzi: Univ. Grenoble Alpes, CNRS, CEA, INRAE, IRIG-LPCV
Michael Hippler: Westfälische Wilhelms Universität
Zoran Nikoloski: University of Potsdam
Jun Minagawa: Division of Environmental photobiology, National Institute for Basic Biology (NIBB)
Arthur R. Grossman: The Carnegie Institution for Science, Department of Plant Biology
Dimitris Petroutsos: Univ. Grenoble Alpes, CNRS, CEA, INRAE, IRIG-LPCV

Nature Communications, 2023, vol. 14, issue 1, 1-12

Abstract: Abstract Photosynthetic algae have evolved mechanisms to cope with suboptimal light and CO2 conditions. When light energy exceeds CO2 fixation capacity, Chlamydomonas reinhardtii activates photoprotection, mediated by LHCSR1/3 and PSBS, and the CO2 Concentrating Mechanism (CCM). How light and CO2 signals converge to regulate these processes remains unclear. Here, we show that excess light activates photoprotection- and CCM-related genes by altering intracellular CO2 concentrations and that depletion of CO2 drives these responses, even in total darkness. High CO2 levels, derived from respiration or impaired photosynthetic fixation, repress LHCSR3/CCM genes while stabilizing the LHCSR1 protein. Finally, we show that the CCM regulator CIA5 also regulates photoprotection, controlling LHCSR3 and PSBS transcript accumulation while inhibiting LHCSR1 protein accumulation. This work has allowed us to dissect the effect of CO2 and light on CCM and photoprotection, demonstrating that light often indirectly affects these processes by impacting intracellular CO2 levels.

Date: 2023
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DOI: 10.1038/s41467-023-37800-6

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