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

Photosynthesis in deserts is challenging since it requires fast adaptation to rapid night-to-day changes, that is, 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 that was isolated from a desert soil crust, and identified the essential functional and structural changes that enable the photosystem to perform photosynthesis under extreme high light conditions. The cryo-electron microscopy structures of PSI from cells grown under low light (PSI_LL) and high light (PSI_HL), obtained at 2.70 and 2.71 Å, respectively, show that part of light-harvesting antenna complex I (LHCI) and the core complex subunit (PsaO) are eliminated from PSI_HL to minimize the photodamage. An additional change is in the pigment composition and their number in LHCI_HL; about 50% of chlorophyll b is replaced by chlorophyll a. This leads to higher electron transfer rates in PSI_HL and might enable C. ohadii PSI to act as a natural photosynthesiser in photobiocatalytic systems. PSI_HL or PSI_LL were attached to an electrode and their induced photocurrent was determined. To obtain photocurrents comparable with PSI_HL, 25 times the amount of PSI_LL was required, demonstrating the high efficiency of PSI_HL. Hence, we suggest that C. ohadii PSI_HL is an ideal candidate for the design of desert artificial photobiocatalytic systems.