Photosystem II (PSII) is essential for energy conversion during oxygenic photosynthesis in plants and algae. Chlorella ohadii, one of the fastest multiplying green algae, thrives under the harsh desert sun but lacks the standard PSII photoprotective mechanisms involving LhcSR/PsbS proteins or protein phosphorylation. Here, we present the cryo-EM structure of the PSII supercomplex from C. ohadii at 2.9 Å resolution, which is used to determine whether the exceptional resistance to desert conditions has a structural basis in PSII. The structure reveals a distinct PsbO isoform and additional subunits, PsbR and PsbY, which enhance core complex stability through extensive interactions. Furthermore, the trimeric light-harvesting complexes (LHCII) are bound to the PSII core by specific light-harvesting proteins whose down-regulation in response to high-light conditions implies a reduction in the number of bound LHCII trimers. These structural modifications, together with the high accumulation of specific polyamines in the thylakoid membrane, play a key role in maintaining PSII stability and photoprotection, allowing C. ohadii to survive in extreme conditions.

Central European Institute of Technology Masaryk University Kamenice 735 5 Brno Czech Republic

Czech Advanced Technology and Research Institute Palacký University Olomouc Šlechtitelů 27 Olomouc Czech Republic

Czech Agrifood Research Center Šlechtitelů 29 Olomouc Czech Republic

Department of Biophysics Faculty of Science Palacký University Šlechtitelů 27 Olomouc Czech Republic

Department of Experimental Biology Faculty of Science Palacký University Olomouc Šlechtitelů 27 Olomouc Czech Republic

Department of Integrative Structural Biochemistry Faculty of Natural Sciences 1 and Biocenter Biosciences Martin Luther University Weinbergweg 22 Halle Germany

Department of Physics and Astronomy and LaserLab Amsterdam Faculty of Science Vrije Universiteit Amsterdam De Boelelaan HV Amsterdam the Netherlands

Institute of Chemical Biology National Hallenic Research Foundation Leof Vasileos Konstantinou 48 Athina 116 35 Athens Greece

Interdisciplinary Research Center HALOmem Charles Tanford Protein Center Martin Luther University Halle Wittenberg Kurt Mothes Straße 3a Halle Germany

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