Evolutionary Loss of the Ability of the Photosystem I Primary Electron Donor for the Redox Interaction with Mn-Bicarbonate Complexes

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V. V. Terentyev^1,a* and S. K. Zharmukhamedov¹

¹Institute of Basic Biological Problems, Pushchino Scientific Center for Biological Research, Russian Academy of Sciences, 142290 Pushchino, Moscow Region, Russia

^* To whom correspondence should be addressed.

Received October 14, 2019; Revised February 21, 2020; Accepted April 3, 2020

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The structure and functional organization of the photosystem I (PSI) reaction center (RC) donor side has a significant similarity to the reaction centers of purple bacteria (bRCs), despite the fact that they belong to different types of RCs. Moreover, the redox potential values of their primary electron donors are identical (~0.5 V). In our earlier reports [Khorobrykh et al. (2008) Phylos. Trans. R. Soc. B., 363, 1245-1251; Terentyev et al. (2011) Biochemistry (Moscow), 76, 1360-1366; Khorobrykh et al. (2018) ChemBioChem, 14, 1725-1731], we have demonstrated redox interaction of low-potential Mn²⁺-bicarbonate complexes with bRCs, which might have been one of the first steps in the evolutionary origin of Mn-cluster of the photosystem II water-oxidizing complex that occurred in the Archean (over 3 billion years ago). In this study, we investigated redox interactions between Mn²⁺-bicarbonate complexes and PSI. Such interactions were almost absent in the original PSI preparations and emerged only in preoxidized PSI preparations containing ~50% oxidized RCs. The interaction between Mn²⁺-bicarbonate complexes and PSI required increased Mn²⁺ concentrations, while its dependence on the HCO₃^– concentration indicated involvement of electroneutral low-potential [Mn(HCO₃)₂] complex in the process. Analysis of the PSI crystal structure revealed steric hindrances on the RC donor side, which could block the redox interaction between Mn²⁺-bicarbonate complexes and oxidized primary electron donor. Comparison of structures of RCs from the PSI and ancient RCs from heliobacteria belonging to the same type of RCs suggested that such hindrances should be absent in the primitive PSI in the Archean and allowed to explain their evolutionary origin as a consequence of PSI RCs into the united electron transport chain (ETC) of the photosynthetic membrane that was accompanied by the evolutionary loss of PSI capacity for the redox interaction with Mn²⁺-bicarbonate complexes.

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KEY WORDS: photosynthesis, evolution of photosynthesis, photosystem I, photosynthetic reaction centers, Mn-bicarbonate complexes

DOI: 10.1134/S0006297920060073

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