15N photo-CIDNP MAS NMR analysis of reaction centers of Chloracidobacterium thermophilum

Abstract

Photochemically induced dynamic nuclear polarization (photo-CIDNP) has been observed in the homodimeric, type-1 photochemical reaction centers (RCs) of the acidobacterium, Chloracidobacterium (Cab.) thermophilum, by 15N magic-angle spinning (MAS) solid-state NMR under continuous white-light illumination. Three light-induced emissive (negative) signals are detected. In the RCs of Cab. thermophilum, three types of (bacterio)chlorophylls have previously been identified: bacteriochlorophyll a (BChl a), chlorophyll a (Chl a), and Zn-bacteriochlorophyll a′ (Zn-BChl a′) (Tsukatani et al. in J Biol Chem 287:5720–5732, 2012). Based upon experimental and quantum chemical 15N NMR data, we assign the observed signals to a Chl a cofactor. We exclude Zn-BChl because of its measured spectroscopic properties. We conclude that Chl a is the primary electron acceptor, which implies that the primary donor is most likely Zn-BChl a′. Chl a and 81-OH Chl a have been shown to be the primary electron acceptors in green sulfur bacteria and heliobacteria, respectively, and thus a Chl a molecule serves this role in all known homodimeric type-1 RCs.

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Acknowledgements

The authors thank Dr. Matthias Findeisen for technical assistence, Eva-Maria Höhn (Group of Professor Dr. Detlev Belder, Universität Leipzig) for the Raman measurements, and Prof. Dr. Stefan Berger (Leipzig) for discussions. J.M. acknowledges the generous support of the Deutsche Forschungsgemeinschaft DFG (MA4972/2-1). Studies in the laboratories of D.A.B. and J.H.G. were supported by Grants DE-FG02-94ER20137 and DE-SC0010575, respectively, from the Photosynthetic Systems Program, Division of Chemical Sciences, Geosciences, and Biosciences (CSGB), Office of Basic Energy Sciences of the U. S. Department of Energy. I.S. is supported by the ERC Starting Grant ‘PhotoMutant’ (678169). Y.L would like to thank Dr. Dror Noy (MIGAL) and his financial support from the ERC (GA 615217) and ISF (GA 558/14).

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Correspondence to Jörg Matysik.

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Zill, J.C., He, Z., Tank, M. et al. 15N photo-CIDNP MAS NMR analysis of reaction centers of Chloracidobacterium thermophilum. Photosynth Res 137, 295–305 (2018). https://doi.org/10.1007/s11120-018-0504-1

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Keywords

  • Chlorophototrophy
  • Reaction centers
  • Chloracidobacterium thermophilum
  • 15N-MAS NMR
  • Photo-CIDNP
  • Zn-BChl a