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

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

doi:10.1038/s41477-021-00983-1

Cited by 30 publications

(23 citation statements)

References 60 publications

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“…Recently, it has been shown that in contrast to the PSI samples of the present study, even a low (2 mM) concentration of ascorbate alone (without any additional mediators) was sufficient to observe the maximal ΔA signal from P + in the case of PSI complex from a desert green microalga Chlorella ohadii grown under high light intensity conditions [54]. On the other hand, PSI particles isolated from the same species but grown under low light conditions required the addition of mediators to show the maximal ΔA signal from P + .…”

Section: Initial Amplitudes Of the P + Decay Kineticscontrasting

confidence: 48%

Competition between intra-protein charge recombination and electron transfer outside photosystem I complexes used for photovoltaic applications

Goyal

Szewczyk

Burdziński

et al. 2022

Photochem Photobiol Sci

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Photosystem I (PSI) complexes isolated from three different species were electrodeposited on FTO conducting glass, forming a photoactive multilayer of the photo-electrode, for investigation of intricate electron transfer (ET) properties in such green hybrid nanosystems. The internal quantum efficiency of photo-electrochemical cells (PEC) containing the PSI-based photo-electrodes did not exceed ~ 0.5%. To reveal the reason for such a low efficiency of photocurrent generation, the temporal evolution of the transient concentration of the photo-oxidized primary electron donor, P+, was studied in aqueous suspensions of the PSI complexes by time-resolved absorption spectroscopy. The results of these measurements provided the information on: (1) completeness of charge separation in PSI reaction centers (RCs), (2) dynamics of internal charge recombination, and (3) efficiency of electron transfer from PSI to the electrolyte, which is the reaction competing with the internal charge recombination in the PSI RC. The efficiency of the full charge separation in the PSI complexes used for functionalization of the electrodes was ~ 90%, indicating that incomplete charge separation was not the main reason for the small yield of photocurrents. For the PSI particles isolated from a green alga Chlamydomonas reinhardtii, the probability of ET outside PSI was ~ 30–40%, whereas for their counterparts isolated from a cyanobacterium Synechocystis sp. PCC 6803 and a red alga Cyanidioschyzon merolae, it represented a mere ~ 4%. We conclude from the transient absorption data for the PSI biocatalysts in solution that the observed small photocurrent efficiency of ~ 0.5% for all the PECs analyzed in this study is likely due to: (1) limited efficiency of ET outside PSI, particularly in the case of PECs based on PSI from Synechocystis and C. merolae, and (2) the electrolyte-mediated electric short-circuiting in PSI particles forming the photoactive layer, particularly in the case of the C. reinhardtii PEC. Graphical abstract

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Section: Initial Amplitudes Of the P + Decay Kineticscontrasting

confidence: 48%

Competition between intra-protein charge recombination and electron transfer outside photosystem I complexes used for photovoltaic applications

Goyal

Szewczyk

Burdziński

et al. 2022

Photochem Photobiol Sci

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“…Yet, this protective carotene accumulated to a much lesser extent than the lutein and the other xanthophylls in the LHC complexes and the free pigment fraction. Unlike the enormous differences between the LL and HL PSII complexes, the difference between the LL and HL PSI-LHCI complexes were minimal, as was also shown before (Fig 7c, Table S3) 48 .…”

Section: Resultssupporting

confidence: 83%

“…Therefore, its photosynthetic properties have been intensively studied in search for new PI protection mechanisms that evolved in this organism, and for their potential implementation in agriculturally valuable plants and algae. These studies revealed that C. ohadii is the fastest growing photosynthetic eukaryote, with a multiplication rate, even at HL intensities, of 1.5-4 h, and exhibits unique changes in its metabolic profile 9,17,21–23,25,48 . In addition, under HL, its photosynthetic activities were modified, partly in PSI 48 , but mostly in PSII 9,25 .…”

Section: Discussionmentioning

confidence: 99%

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A desert green alga that thrives at extreme high-light intensities using a unique photoin-hibition protection mechanism

Levin

Yasmin

Simanowitz

et al. 2022

Preprint

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While light is the driving force of photosynthesis, excessive light can be harmful. Photoinhibi-tion, or light-induced photo-damage, is one of the key processes limiting photosynthesis. When the absorbed light exceeds the amount that can be dissipated by photosynthetic elec-tron flow and other processes, damaging radicals are formed that mostly inactivate photosys-tem II (PSII). A well-defined mechanism that protects the photosynthetic apparatus from photoinhibition has been described in the model green alga Chlamydomonas reinhardtii and plants. Chlorella ohadii is a green micro-alga, isolated from biological desert soil crusts, that thrives under extreme high light (HL) in which other organisms do not survive. Here, we show that this alga evolved unique protection mechanisms distinct from those of C. reinhard-tii and plants. When grown under extreme HL, significant structural changes were noted in the C. ohadii thylakoids, including a drastic reduction in the antennae and the formation of stripped core PSII, lacking its outer and inner antennae. This is accompanied by a massive ac-cumulation of protective carotenoids and proteins that scavenge harmful radicals. At the same time, several elements central to photoinhibition protection in C. reinhardtii, such as psbS, the stress-related light harvesting complex, PSII protein phosphorylation and state-transitions are entirely absent or were barely detected in C. ohadii. Taken together, a unique photoinhibition protection mechanism evolved in C. ohadii, enabling the species to thrive under extreme-light intensities where other photosynthetic organisms fail to survive.

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“…In BPECs, photosynthesis is harnessed to convert the light energy to electricity or to produce high-energy chemical compounds. BPECs can utilize isolated photosynthetic components such as thylakoid membranes ( Pinhassi et al, 2016 ), chloroplasts ( Hasan et al, 2017 ), photosystem I (PSI; Gizzie et al, 2015 ; Caspy et al, 2021 ; Toporik et al, 2021 ; Wang et al, 2022 ), photosystem II (PSII; Sokol et al, 2018 ; Hartmann et al, 2020 ; Zhang and Erwin, 2020 ; Shoyhet et al, 2021 ) or intact living photosynthetic microorganisms ( Shlosberg et al, 2021b ; Bombelli et al, 2022 ; De Moura Torquato and Grattieri, 2022 ). Unlike non-photosynthetic bacteria, the photosynthetic organisms possess the mechanisms needed to utilize sun light and convert it to electricity ( Chen and Blankenship, 2021 ).…”

Section: Introductionmentioning

confidence: 99%

Harnessing photosynthesis to produce electricity using cyanobacteria, green algae, seaweeds and plants

2022

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The conversion of solar energy into electrical current by photosynthetic organisms has the potential to produce clean energy. Life on earth depends on photosynthesis, the major mechanism for biological conversion of light energy into chemical energy. Indeed, billions of years of evolution and adaptation to extreme environmental habitats have resulted in highly efficient light-harvesting and photochemical systems in the photosynthetic organisms that can be found in almost every ecological habitat of our world. In harnessing photosynthesis to produce green energy, the native photosynthetic system is interfaced with electrodes and electron mediators to yield bio-photoelectrochemical cells (BPECs) that transform light energy into electrical power. BPECs utilizing plants, seaweeds, unicellular photosynthetic microorganisms, thylakoid membranes or purified complexes, have been studied in attempts to construct efficient and non-polluting BPECs to produce electricity or hydrogen for use as green energy. The high efficiency of photosynthetic light-harvesting and energy production in the mostly unpolluting processes that make use of water and CO2 and produce oxygen beckons us to develop this approach. On the other hand, the need to use physiological conditions, the sensitivity to photoinhibition as well as other abiotic stresses, and the requirement to extract electrons from the system are challenging. In this review, we describe the principles and methods of the different kinds of BPECs that use natural photosynthesis, with an emphasis on BPECs containing living oxygenic photosynthetic organisms. We start with a brief summary of BPECs that use purified photosynthetic complexes. This strategy has produced high-efficiency BPECs. However, the lifetimes of operation of these BPECs are limited, and the preparation is laborious and expensive. We then describe the use of thylakoid membranes in BPECs which requires less effort and usually produces high currents but still suffers from the lack of ability to self-repair damage caused by photoinhibition. This obstacle of the utilization of photosynthetic systems can be significantly reduced by using intact living organisms in the BPEC. We thus describe here progress in developing BPECs that make use of cyanobacteria, green algae, seaweeds and higher plants. Finally, we discuss the future challenges of producing high and longtime operating BPECs for practical use.

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

Cited by 30 publications

References 60 publications

Competition between intra-protein charge recombination and electron transfer outside photosystem I complexes used for photovoltaic applications

Competition between intra-protein charge recombination and electron transfer outside photosystem I complexes used for photovoltaic applications

A desert green alga that thrives at extreme high-light intensities using a unique photoin-hibition protection mechanism

Harnessing photosynthesis to produce electricity using cyanobacteria, green algae, seaweeds and plants

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