ILANIT 2023

Cryo-EM PSI structure reveals adaptation mechanisms to extreme high light in Chlorella ohadii

Ehud Neumann 1 Ido Caspy 2 Maria Fadeeva 2 Varda Liveanu 3 Anton Savitsky 4,8 Anna Frank 5 Yael Levi Kalisman 6 Yoel Shkolnisky 2 Omer Murik 1 Haim Treves 1 Volker Hartmann 5 Marc Nowaczyk 5 Wolfgang Schuhmann 7 Matthias Rögner 5 Itamar Willner 1 Aaron Kaplan 1 Gadi Schuster 3 Nathan Nelson 2 Wolfgang Lubitz 8 Rachel Nechushtai 1
1Institute of Life Science, The Hebrew University of Jerusalem, Israel
2Department of Biochemistry, Tel Aviv University, Israel
3Faculty of Biology, Technion—Israel Institute of Technology, Israel
4Faculty of Physics, Technical University of Dortmund, Germany
5Biology & Biotechnology, Ruhr University Bochum, Germany
6The Center for Nanoscience and Nanotechnology, The Hebrew University of Jerusalem, Israel
7Faculty of Chemistry and Biochemistry, Ruhr University Bochum, Germany
8Chemical Energy Conversion, Max Planck Institute, Germany

Photosynthesis in the deserts is challenging since it requires rapid adaptation from dawn’s low light (LL) to extreme high light (HL) intensities during the daytime. To understand these adaptation mechanisms, we purified Photosystem I (PSI) from Chlorella ohadii, a green alga isolated from the desert’s soil’s crust, and identified the essential functional and structural changes that enable the photosystem to perform photosynthesis under extreme HL conditions. The Cryo-EM structures of PSI from cells grown under LL (PSILL) and HL (PSIHL), obtained at 2.70 and 2.71 Å, respectively, show that changes in both the light-harvesting antenna complex I (LHCI) and the core complex (CC) subunit occur in order to minimise the photodamage. In the CC, the CC subunit PsaO is eliminated from PSIHL, preventing state transition. In the LHCI, the main change is found at the pigment composition of LHCIHL; about 50% of chlorophyll b is replaced by chlorophyll a. This leads to higher electron transfer (ET) rates in PSIHL and might enable C. ohadii PSI to act as a natural photosynthesiser in photobiocatalytic systems. PSIHL or PSILL were attached to an electrode and their induced photocurrent was determined. 25-times the amount of PSILL was required to obtain photocurrents comparable to PSIHL, demonstrating the high efficiency of PSIHL. Hence, we suggest that C. ohadii PSIHL is an ideal candidate for the design of desert artificial photobiocatalytic systems.