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Comparative ENDOR study at 34 GHz of the triplet state of the primary donor in bacterial reaction centers of Rb. sphaeroides and Bl. viridis

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Abstract

The primary electron donor (P) in the photosynthetic bacterial reaction center of Rhodobacter sphaeroides and Blastochloris viridis consists of a dimer of bacteriochlorophyll a and b cofactors, respectively. Its photoexcited triplet state in frozen solution has been investigated by time resolved ENDOR spectroscopy at 34 GHz. The observed ENDOR spectra for 3P865 and 3P960 are essentially the same, indicating very similar spin density distributions. Exceptions are the ethylidene groups unique to the bacteriochlorophyll b dimer in 3P960. Strikingly, the observed hyperfine coupling constants of the ethylidene groups are larger than in the monomer, which speaks for an asymmetrically delocalized wave function over both monomer halves in the dimer. The latter observation corroborates previous findings of the spin density in the radical cation states P •+865 (Lendzian et al. in Biochim Biophys Acta 1183:139–160, 1993) and P •+960 (Lendzian et al. in Chem Phys Lett 148:377–385, 1988). As compared to the bacteriochlorophyll monomer, the hyperfine coupling constants of the methyl groups 21 and 121 are reduced by at least a factor of two, and quantitative analysis of these couplings gives rise to a ratio of approximately 3:1 for the spin density on the halves PL:PM. Our findings are discussed in light of the large difference in photosynthetic activity of the two branches of cofactors present in the bacterial reaction center proteins.

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Notes

  1. In an alternate description, the triplet state of the primary donor can be described as a combination of two local excitations 3PLPM, P 3L PM and charge transfer states P + L P − M and P − L P + M ; however, the weight contribution of individual terms in the wavefunction is unknown (Lendzian et al. 1998; Thurnauer 1979).

Abbreviations

Bl. :

Blastochloris

bRC:

Bacterial reaction center

BChl a :

Bacteriochlorophyll a

BChl b :

Bacteriochlorophyll b

BPheo:

Bacteriopheophytin

DFT:

Density functional theory

EPR:

Electron paramagnetic resonance

ENDOR:

Electron nuclear double resonance

GGA:

Generalized gradient approximation

HOMO:

Highest occupied molecular orbital

LUMO:

Lowest unoccupied molecular orbital

P:

Primary donor

P865 :

Primary donor in Rhodobacter sphaeroides

P960 :

Primary donor in Blastochloris viridis

Q:

Quinone

Rb. :

Rhodobacter

SCF:

Self-consistent field

ZFS:

Zero field splitting

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Acknowledgments

The authors thank Prof. Dr. K. Möbius for helpful discussions and G. Schmitz and K. Wrede (MPI CEC) for their help with the purification of reaction centers of Rb. sphaeroides R.26.1 and Bl. viridis wild type. H. Selbach and M. Reus (MPI CEC) are thanked for their help and kind advice at various stages of the preparations. This project was supported by the DFG-NWO international collaborative research grant project GA1100/1-2 and the MPG.

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Authors and Affiliations

  1. Max-Planck-Institut für Chemische Energiekonversion, Stiftstrasse 34-36, 45470, Mülheim an der Ruhr, Germany

    Aliaksandr Marchanka, Wolfgang Lubitz & Maurice van Gastel

  2. European Molecular Biology Laboratory (EMBL) Structural and Computational Biology Unit, Meyerhofstrasse 1, 69117, Heidelberg, Germany

    Aliaksandr Marchanka

  3. Freie Universität Berlin, Fachbereich Physik, Arnimallee 14, 14195, Berlin, Germany

    Martin Plato

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  1. Aliaksandr Marchanka
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  2. Wolfgang Lubitz
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  4. Maurice van Gastel
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Correspondence to Wolfgang Lubitz.

Electronic supplementary material

Full dataset of hyperfine couplings from the ENDOR spectra and DFT calculations. This material is available free of charge via the Internet at http://www.springerlink.com.

Supplementary material 1 (DOCX 40 kb)

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Marchanka, A., Lubitz, W., Plato, M. et al. Comparative ENDOR study at 34 GHz of the triplet state of the primary donor in bacterial reaction centers of Rb. sphaeroides and Bl. viridis . Photosynth Res 120, 99–111 (2014). https://doi.org/10.1007/s11120-012-9786-x

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