1. Impaired photoprotection in Phaeodactylum tricornutum KEA3 mutants reveals the proton regulatory circuit of diatoms light acclimation
- Author
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Seydoux, Claire, Storti, Mattia, Giovagnetti, Vasco, Matuszyńska, Anna, Guglielmino, Erika, Zhao, Xue, Giustini, Cécile, Pan, Yufang, Blommaert, Lander, Angulo, Jhoanell, Ruban, Alexander V., Hu, Hanhua, Bailleul, Benjamin, Courtois, Florence, Allorent, Guillaume, Finazzi, Giovanni, Light Photosynthesis & Metabolism (Photosynthesis), Physiologie cellulaire et végétale (LPCV), Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche Interdisciplinaire de Grenoble (IRIG), Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Grenoble Alpes (UGA)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche Interdisciplinaire de Grenoble (IRIG), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Grenoble Alpes (UGA), Queen Mary University of London (QMUL), Rheinisch-Westfälische Technische Hochschule Aachen University (RWTH), Institute of Hydrobiology [Wuhan], Chinese Academy of Sciences [Beijing] (CAS), Biologie du chloroplaste et perception de la lumière chez les micro-algues, Institut de biologie physico-chimique (IBPC (FR_550)), Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS), HFSP ‘Photosynthesis light utilization dynamics and ion fluxes: making the link’, CNRS ‘Momentum’ program, The Leverhulme Trust (RPG-2018-199), The Biotechnology and Biological Sciences Research Council (BB/R015694/1), The Royal Society Wolfson Research Merit Award (WM140084), Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) under Germany’s Excellence Strategy – EXC-2048/1 – project ID 390686111 and DFG Research Grant MA 8103/1-1, Strategic Priority Research Program of the Chinese Academy of Sciences (no. XDPB18), ANR-10-LABX-0049,GRAL,Grenoble Alliance for Integrated Structural Cell Biology(2010), ANR-17-EURE-0003,CBH-EUR-GS,CBH-EUR-GS(2017), ANR-17-CE05-0029,MoMix,Modélisation de la Mixotrophie chez l'algue extrêmophile Galdieria sulphuraria(2017), European Project: 833184, ChloroMito, and European Project: 715579,PhotoPHYTOMICS
- Subjects
photosynthesis ,Light ,Physiology ,Acclimatization ,fungi ,proton motive force ,Light-Harvesting Protein Complexes ,ion channels ,Plant Science ,diatoms ,nonphotochemical quenching ,[SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology ,phytoplankton ,[SDV.BBM]Life Sciences [q-bio]/Biochemistry, Molecular Biology ,Protons - Abstract
International audience; Diatoms are successful phytoplankton clades able to acclimate to changing environmental conditions, including e.g. variable light intensity. Diatoms are outstanding at dissipating light energy exceeding the maximum photosynthetic electron transfer (PET) capacity via the nonphotochemical quenching (NPQ) process. While the molecular effectors of NPQ as well as the involvement of the proton motive force (PMF) in its regulation are known, the regulators of the PET/PMF relationship remain unidentified in diatoms. We generated mutants of the H$^+$ /K$^+$ antiporter KEA3 in the model diatom $Phaeodactylum\ tricornutum$. Loss of KEA3 activity affects the PET/PMF coupling and NPQ responses at the onset of illumination, during transients and in steady-state conditions. Thus, this antiporter is a main regulator of the PET/PMF coupling. Consistent with this conclusion, a parsimonious model including only two free components, KEA3 and the diadinoxanthin de-epoxidase, describes most of the feedback loops between PET and NPQ. This simple regulatory system allows for efficient responses to fast (minutes) or slow (e.g. diel) changes in light environment, thanks to the presence of a regulatory calcium ion (Ca$^{2+}$ )-binding domain in KEA3 modulating its activity. This circuit is likely tuned by the NPQ-effector proteins, LHCXs, providing diatoms with the required flexibility to thrive in different ocean provinces.
- Published
- 2022