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

Ido Caspy; Ehud Neumann; Maria Fadeeva; Varda Liveanu; Anton Savitsky; Anna Frank; Yael Levi Kalisman; Yoel Shkolnisky; Omer Murik; Haim Treves; Volker Hartmann; Marc M. Nowaczyk; Wolfgang Schuhmann; Matthias Rögner; Itamar Willner; Aaron Kaplan; Gadi Schuster; Nathan Nelson; Wolfgang Lubitz; Rachel Nechushtai

doi:10.1038/s41477-021-00983-1

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

Ido Caspy, Ehud Neumann, Maria Fadeeva, Varda Liveanu, Anton Savitsky, Anna Frank, Yael Levi Kalisman, Yoel Shkolnisky, Omer Murik, Haim Treves, Volker Hartmann, Marc M. Nowaczyk, Wolfgang Schuhmann, Matthias Rögner, Itamar Willner, Aaron Kaplan, Gadi Schuster, Nathan Nelson^*, Wolfgang Lubitz^*, Rachel Nechushtai^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

20 Scopus citations

Abstract

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.

Original language	English
Pages (from-to)	1314-1322
Number of pages	9
Journal	Nature Plants
Volume	7
Issue number	9
DOIs	https://doi.org/10.1038/s41477-021-00983-1
State	Published - Sep 2021

Bibliographical note

Funding Information:
This work was supported by the Deutsche Forschungsgemeinschaft (AD 458/1-1 and LU 315/17-1) in the framework of a Deutsch–Israelische Projektkooperation, ‘Nanoengineered optobioelectronics with biomaterials and bioinspired assemblies’. W.L. and A.S. thank the Max Planck Society for their financial support. This study was part of the research in the MINERVA Centre for Bio-hybrid Complex Systems. We thank the Electron Microscopy Core Facility at the EMBL for their support. E.N. was supported by the Hebrew University of Jerusalem - Prof. Leonora Reinhold Fellowship. A.F. and M.M.N. were supported by the Research Training Group 2341 ‘MiCon’ also funded by the DFG. We thank F. Weis for his assistance and guidance in data collection. Molecular graphics and analyses were performed with UCSF Chimera, developed by the Resource for Biocomputing, Visualization and Informatics at the University of California San Francisco, with support from National Institutes of Health P41-GM103311. This work was supported by The Israel Science Foundation (grant no. 569/17) to N.N. and by the German–Israeli Foundation for Scientific Research and Development to N.N., grant no. G-1483-207/2018. Y.S. was supported by the European Research Council under the European Union’s Horizon 2020 research and innovation programme (grant agreement 723991—CRYOMATH) and by the Zimin Institute for Engineering Solutions Advancing Better Lives. G.S. acknowledges funding by a ‘Nevet’ grant from the Grand Technion Energy Program and a Technion Vice President of Research (VPR) Berman Grant for Energy Research.

Publisher Copyright:
© 2021, The Author(s), under exclusive licence to Springer Nature Limited.

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Caspy, I., Neumann, E., Fadeeva, M., Liveanu, V., Savitsky, A., Frank, A., Kalisman, Y. L., Shkolnisky, Y., Murik, O., Treves, H., Hartmann, V., Nowaczyk, M. M., Schuhmann, W., Rögner, M., Willner, I., Kaplan, A., Schuster, G., Nelson, N., Lubitz, W., & Nechushtai, R. (2021). Cryo-EM photosystem I structure reveals adaptation mechanisms to extreme high light in Chlorella ohadii. Nature Plants, 7(9), 1314-1322. https://doi.org/10.1038/s41477-021-00983-1

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

abstract = "Photosynthesis in deserts is challenging since it requires fast adaptation to rapid night-to-day changes, that is, from dawn{\textquoteright}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 (PSILL) and high light (PSIHL), obtained at 2.70 and 2.71 {\AA}, respectively, show that part of light-harvesting antenna complex I (LHCI) and the core complex subunit (PsaO) are eliminated from PSIHL to minimize the photodamage. An additional change is in the pigment composition and their number in LHCIHL; about 50% of chlorophyll b is replaced by chlorophyll a. This leads to higher electron transfer 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. To obtain photocurrents comparable with PSIHL, 25 times the amount of PSILL was required, 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.",

author = "Ido Caspy and Ehud Neumann and Maria Fadeeva and Varda Liveanu and Anton Savitsky and Anna Frank and Kalisman, {Yael Levi} and Yoel Shkolnisky and Omer Murik and Haim Treves and Volker Hartmann and Nowaczyk, {Marc M.} and Wolfgang Schuhmann and Matthias R{\"o}gner and Itamar Willner and Aaron Kaplan and Gadi Schuster and Nathan Nelson and Wolfgang Lubitz and Rachel Nechushtai",

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month = sep,

doi = "10.1038/s41477-021-00983-1",

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Caspy, I, Neumann, E, Fadeeva, M, Liveanu, V, Savitsky, A, Frank, A, Kalisman, YL, Shkolnisky, Y, Murik, O, Treves, H, Hartmann, V, Nowaczyk, MM, Schuhmann, W, Rögner, M, Willner, I, Kaplan, A, Schuster, G, Nelson, N, Lubitz, W & Nechushtai, R 2021, 'Cryo-EM photosystem I structure reveals adaptation mechanisms to extreme high light in Chlorella ohadii', Nature Plants, vol. 7, no. 9, pp. 1314-1322. https://doi.org/10.1038/s41477-021-00983-1

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AU - Caspy, Ido

AU - Neumann, Ehud

AU - Fadeeva, Maria

AU - Liveanu, Varda

AU - Savitsky, Anton

AU - Frank, Anna

AU - Kalisman, Yael Levi

AU - Shkolnisky, Yoel

AU - Murik, Omer

AU - Treves, Haim

AU - Hartmann, Volker

AU - Nowaczyk, Marc M.

AU - Schuhmann, Wolfgang

AU - Rögner, Matthias

AU - Willner, Itamar

AU - Kaplan, Aaron

AU - Schuster, Gadi

AU - Nelson, Nathan

AU - Lubitz, Wolfgang

AU - Nechushtai, Rachel

PY - 2021/9

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N2 - 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 (PSILL) and high light (PSIHL), 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 PSIHL to minimize the photodamage. An additional change is in the pigment composition and their number in LHCIHL; about 50% of chlorophyll b is replaced by chlorophyll a. This leads to higher electron transfer 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. To obtain photocurrents comparable with PSIHL, 25 times the amount of PSILL was required, 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.

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

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