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Dehydration affects the electronic structure of the primary electron donor in bacterial photosynthetic reaction centers: evidence from visible-NIR and light-induced difference FTIR spectroscopy

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Abstract

The photosynthetic reaction center (RC) is a membrane pigment—protein complex that catalyzes the initial charge separation reactions of photosynthesis. Following photoexcitation, the RC undergoes conformational relaxations which stabilize the charge-separated state. Dehydration of the complex inhibits its conformational dynamics, providing a useful tool to gain insights into the relaxational processes. We analyzed the effects of dehydration on the electronic structure of the primary electron donor P, as probed by visible-NIR and light-induced FTIR difference spectroscopy, in RC films equilibrated at different relative humidities r. Previous FTIR and ENDOR spectroscopic studies revealed that P, an excitonically coupled dimer of bacteriochlorophylls, can be switched between two conformations, P866 and P850, which differ in the extent of delocalization of the unpaired electron between the two bacteriochlorophyll moieties (PL and PM) of the photo-oxidized radical P+. We found that dehydration (at r = 11%) shifts the optical Qy band of P from 866 to 850845_ nm, a large part of the effect occurring already at r = 76%. Such a dehydration weakens light-induced difference FTIR marker bands, which probe the delocalization of charge distribution within the P+ dimer (the electronic band of P+ at 2700 cm−1, and the associated phase-phonon vibrational modes at around 1300, 1480, and 1550 cm−1). From the analysis of the P+ keto C?O bands at 1703 and 1713-15 cm−1, we inferred that dehydration induces a stronger localization of the unpaired electron on PL+. The observed charge redistribution is discussed in relation to the dielectric relaxation of the photoexcited RC on a long (102 s) time scale.

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Abbreviations

BChl:

Bacteriochlorophyll

Bphe:

Bacteriopheophytin

CTAB:

Cetyl-trimethyl-ammonium bromide

ENDOR:

Electron nuclear double resonance

EPR:

Electron paramagnetic resonance

FTIR:

Fourier transform infrared

HOMO:

Highest occupied molecular orbital

LDAO:

Lauryldimethylamine N-oxide

MO:

Molecular orbital

NIR:

Near infrared

P:

Primary donor

QA,B:

Quinones in the RC

Qy:

Optical transition in BChls

Rb. :

Rhodobacter

RC:

Reaction center

TRIPLE:

Electron-nuclear-nuclear triple resonance

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Authors and Affiliations

  1. Dipartimento di Farmacia e Biotecnologie, FaBiT, Università di Bologna, Bologna, Italy

    Marco Malferrari, Francesco Francia & Giovanni Venturoli

  2. Dipartimento di Scienze Biologiche, Geologiche e Ambientali, BiGeA, Università di Bologna, Bologna, Italy

    Paola Turina

  3. LASIR, UMR 8516, Université Lille 1, Cité Scientifique, 59655, Villeneuve d’Ascq, France

    Alberto Mezzetti

  4. Service de Bioénergétique, Biologie Structurale et Mécanismes UMR 8221, IBITeC-S, Bat 532, CEA-Saclay, 91191, Gif-sur-Yvette, France

    Alberto Mezzetti & Winfried Leibl

  5. Consorzio Nazionale Interuniversitario per le Scienze Fisiche della Materia (CNISM), c/o Dipartimento di Fisica e Astronomia, DIFA, Università di Bologna, Bologna, Italy

    Giovanni Venturoli

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  1. Marco Malferrari
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  2. Paola Turina
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Malferrari, M., Turina, P., Francia, F. et al. Dehydration affects the electronic structure of the primary electron donor in bacterial photosynthetic reaction centers: evidence from visible-NIR and light-induced difference FTIR spectroscopy. Photochem Photobiol Sci 14, 238–251 (2015). https://doi.org/10.1039/c4pp00245h

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