A1 Refereed original research article in a scientific journal
Flavodiiron proteins associate pH-dependently with the thylakoid membrane for ferredoxin-1-powered O2 photoreduction
Authors: Nikkanen, Lauri; Vakal, Serhii; Hubáček, Michal; Santana-Sánchez, Anita; Konert, Grzegorz; Wang, Yingying; Boehm, Marko; Gutekunst, Kirstin; Salminen, Tiina A.; Allahverdiyeva, Yagut
Publisher: WILEY
Publishing place: HOBOKEN
Publication year: 2025
Journal: New Phytologist
Journal name in source: NEW PHYTOLOGIST
Journal acronym: NEW PHYTOL
Volume: 246
Issue: 5
First page : 2084
Last page: 2101
Number of pages: 18
ISSN: 0028-646X
eISSN: 1469-8137
DOI: https://doi.org/10.1111/nph.70114
Web address : https://doi.org/10.1111/nph.70114
Flavodiiron proteins (FDPs) catalyse light-dependent reduction of oxygen to water in photosynthetic organisms, creating an electron sink on the acceptor side of Photosystem I that protects the photosynthetic apparatus. However, ambiguity about the electron donor(s) remains, and the molecular mechanisms regulating FDP activity have remained elusive.
We employed spectroscopic and gas flux analysis of photosynthetic electron transport, bimolecular fluorescence complementation assays for in vivo protein-protein interactions in the model cyanobacterium Synechocystis sp. PCC 6803, and in silico surface charge modelling.
We demonstrated that ferredoxin-1 interacts with Flv1, Flv2, and Flv3, and is the main electron donor to FDP heterooligomers, which are responsible for the photoreduction of oxygen. Moreover, we revealed that FDP heterooligomers dissociate from the thylakoid membrane upon alkalisation of the cytosol, providing the first in vivo evidence of a self-regulatory feedback mechanism allowing dynamic control of FDP activity and maintenance of photosynthetic redox balance in fluctuating environments.
Our findings have direct implications for rationally directing electron flux towards desired reactions in biotechnological applications.
Funding information in the publication:
We thank Pauli Kallio for kindly providing plasmids for modular cloning and for helpful discussions, Laura Wey for valuable discussions, and Anniina Lepisto, Janette Vahasarja, Sofia Westerlund, Ville Kapyla, Mahfuzur Rahman, and Linda Nevala for technical assistance. Biophysical experiments were performed within the PHOTOSYN infrastructure at the University of Turku, and confocal microscopy at the Cell Imaging and Cytometry Core, Turku Bioscience Centre, with the support of Biocenter Finland. We also thank the bioinformatics (JV Lehtonen), translational activities, and structural biology FINStruct infrastructure support from Biocenter Finland and CSC IT Center for Science for computational infrastructure support at the Structural Bioinformatics Laboratory (SBL), Abo Akademi University. Research was funded by Research Council of Finland projects 'Revisiting Photosynthesis' (no. 315119 to YA), 'Channelling photosynthesis' (no. 354876 to LN), the NordForsk Nordic Center of Excellence 'NordAqua' (no. 82845 to YA), the Novo Nordisk Fonden 'PhotoCat' (no. NNF20OC0064371 to YA), and the China Scholarship Council (CSC) (grant no. 201406320187 to YW).
