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High-pressure tuning of primary photochemistry in bacterial photosynthesis: membrane-bound versus detergent-isolated reaction centers

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Abstract

While photosynthesis thrives at close to normal pressures and temperatures, it is presently well known that life is similarly commonplace in the hostile environments of the deep seas as well as around hydrothermal vents. It is thus imperative to understand how key biological processes perform under extreme conditions of high pressures and temperatures. Herein, comparative steady-state and picosecond time-resolved spectroscopic studies were performed on membrane-bound and detergent-purified forms of a YM210W mutant reaction center (RC) from Rhodobacter sphaeroides under modulating conditions of high hydrostatic pressure applied at ambient temperature. A previously established breakage of the lone hydrogen bond formed between the RC primary donor and the protein scaffold was shown to take place in the membrane-bound RC at an almost 3 kbar higher pressure than in the purified RC, confirming the stabilizing role of the lipid environment for membrane proteins. The main change in the multi-exponential decay of excited primary donor emission across the experimental 10 kbar pressure range involved an over two-fold continuous acceleration, the kinetics becoming increasingly mono-exponential. The fastest component of the emission decay, thought to be largely governed by the rate of primary charge separation, was distinctly slower in the membrane-bound RC than in the purified RC. The change in character of the emission decay with pressure was explained by the contribution of charge recombination to emission decreasing with pressure as a result of an increasing free energy gap between the charge-separated and excited primary donor states. Finally, it was demonstrated that, in contrast to a long-term experimental paradigm, adding a combination of sodium ascorbate and phenazine methosulfate to the protein solution potentially distorts natural photochemistry in bacterial RCs.

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Acknowledgements

Financial support provided by the Estonian Research Council (grants PRG539, PRG664, and PSG264), the ESF DoRa 4 program (grant NLOFY12523T), and the H2020-MSCA-RISE-2015 program (grant 690853) is greatly appreciated.

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Authors and Affiliations

  1. Institute of Physics, University of Tartu, W. Ostwald Str. 1, Tartu, 50411, Estonia

    Kõu Timpmann, Erko Jalviste, Manoop Chenchiliyan, Liina Kangur & Arvi Freiberg

  2. School of Biochemistry, Biomedical Sciences Building, University of Bristol, University Walk, Bristol, BS8 1TD, UK

    Michael R. Jones

  3. Institute of Molecular and Cell Biology, University of Tartu, Riia 23, Tartu, 51010, Estonia

    Arvi Freiberg

  4. Estonian Academy of Sciences, Kohtu 6, Tallinn, 10130, Estonia

    Arvi Freiberg

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  1. Kõu Timpmann
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  2. Erko Jalviste
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Correspondence to Arvi Freiberg.

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Timpmann, K., Jalviste, E., Chenchiliyan, M. et al. High-pressure tuning of primary photochemistry in bacterial photosynthesis: membrane-bound versus detergent-isolated reaction centers. Photosynth Res 144, 209–220 (2020). https://doi.org/10.1007/s11120-020-00724-z

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