Modulation of cyanobacterial Photosystem I protein environment and spectral capacity in response to changes in electron flow pathways and photon flux

Smolinski, Sharon L.; Tokmina-Lukaszewska, Monika; Holland, Junia M.; Guo, Zhanjun; Kisgeropoulos, Effie; Bothner, Brian; King, Paul W.; Lubner, Carolyn E.

doi:10.1016/j.jbc.2025.110233

Modulation of cyanobacterial Photosystem I protein environment and spectral capacity in response to changes in electron flow pathways and photon flux

Journal Article · Wed May 14 00:00:00 EDT 2025 · Journal of Biological Chemistry

DOI:https://doi.org/10.1016/j.jbc.2025.110233· OSTI ID:2566310

^[1]; ^[2]; Holland, Junia M. ^[2]; Guo, Zhanjun ^[1]; ^[1]; ^[1]; ^[1];

National Renewable Energy Laboratory (NREL), Golden, CO (United States)
Montana State Univ., Bozeman, MT (United States)

Cyanobacterial photosystem I (PSI) can undergo modifications that adjust photosynthetic electron transport in response to fluctuations in environmental and cellular conditions. We recently reported that PSI isolated from Synechocystis sp. PCC 6803 (S. 6803) strains lacking a peripheral oxygen reduction reaction (ORR1) pathway demonstrated altered P₇₀₀ photooxidation capacity, changes in spectral properties, and a higher proportion of monomers. These changes in PSI were augmented when cells were grown under higher photon flux, which creates a greater energy imbalance at PSI. We have shown that the modified PSI is functional in photochemical charge separation and ferredoxin reduction reactions. Thus, we hypothesized that monomerization of PSI was caused by changes in the environment of PsaL, which is known to be essential for stabilizing trimers. To test our hypothesis, we isolated PSI monomers and trimers from ORR1 and wild-type (WT) strains. The electron paramagnetic resonance (EPR) spectra of reduced PSI demonstrated the presence of intact F_A and F_B [4Fe-4S] clusters, consistent with measurements of functional charge separation and electron transport. Limited proteolysis followed by mass spectrometric analysis showed altered accessibility of PsaL in the ORRI PSI monomers compared to WT monomers, and included regions associated with chlorophyll and carotenoid binding, and in functional interactions with adjacent subunits. In addition, ORR1 PSI monomers had spectral changes compared to WT PSI due to differences in carotenoid compositions. Collectively, these findings reveal new insights into how microbes adjust PSI structure and photochemistry to mitigate photodamage in response to changes in electron utilization by downstream chemical reactions.

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Research Organization:: National Renewable Energy Laboratory (NREL), Golden, CO (United States)

Sponsoring Organization:: National Institutes of Health (NIH); USDOE; USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division

Grant/Contract Number:: AC36-08GO28308

OSTI ID:: 2566310

Alternate ID(s):: OSTI ID: 2586529

Report Number(s):: NREL/JA--2700-86563

Journal Information:: Journal of Biological Chemistry, Journal Name: Journal of Biological Chemistry Journal Issue: 7 Vol. 301; ISSN 0021-9258

Publisher:: Elsevier BVCopyright Statement

Country of Publication:: United States

Language:: English

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Modulation of cyanobacterial Photosystem I protein environment and spectral capacity in response to changes in electron flow pathways and photon flux

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