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

Jeremias C. Zill; Zhihui He; Marcus Tank; Bryan H. Ferlez; Daniel P. Canniffe; Yigal Lahav; Peter Bellstedt; A. Alia; Igor Schapiro; John H. Golbeck; Donald A. Bryant; Jörg Matysik

doi:10.1007/s11120-018-0504-1

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

Jeremias C. Zill, Zhihui He, Marcus Tank, Bryan H. Ferlez, Daniel P. Canniffe, Yigal Lahav, Peter Bellstedt, A. Alia, Igor Schapiro, John H. Golbeck, Donald A. Bryant, Jörg Matysik^*

^*Corresponding author for this work

Institute of Chemistry

Research output: Contribution to journal › Article › peer-review

16 Scopus citations

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.

Original language	American English
Pages (from-to)	295-305
Number of pages	11
Journal	Photosynthesis Research
Volume	137
Issue number	2
DOIs	https://doi.org/10.1007/s11120-018-0504-1
State	Published - 1 Aug 2018

Bibliographical note

Funding Information:
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).

Funding Information:
The authors thank Dr. Matthias Findeisen for technical assistence, Eva-Maria H?hn (Group of Professor Dr. Detlev Belder, Universit?t 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).

Publisher Copyright:
© 2018, Springer Science+Business Media B.V., part of Springer Nature.

Keywords

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

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10.1007/s11120-018-0504-1

Cite this

@article{d2c51c79696745998d485255496143da,

title = "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.",

keywords = "Chloracidobacterium thermophilum, Chlorophototrophy, N-MAS NMR, Photo-CIDNP, Reaction centers, Zn-BChl a′",

author = "Zill, {Jeremias C.} and Zhihui He and Marcus Tank and Ferlez, {Bryan H.} and Canniffe, {Daniel P.} and Yigal Lahav and Peter Bellstedt and A. Alia and Igor Schapiro and Golbeck, {John H.} and Bryant, {Donald A.} and J{\"o}rg Matysik",

note = "Funding Information: Acknowledgements The authors thank Dr. Matthias Findeisen for technical assistence, Eva-Maria H{\"o}hn (Group of Professor Dr. Detlev Belder, Universit{\"a}t 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 {\textquoteleft}PhotoMutant{\textquoteright} (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). Funding Information: The authors thank Dr. Matthias Findeisen for technical assistence, Eva-Maria H?hn (Group of Professor Dr. Detlev Belder, Universit?t 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). Publisher Copyright: {\textcopyright} 2018, Springer Science+Business Media B.V., part of Springer Nature.",

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doi = "10.1007/s11120-018-0504-1",

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T1 - 15N photo-CIDNP MAS NMR analysis of reaction centers of Chloracidobacterium thermophilum

AU - Zill, Jeremias C.

AU - He, Zhihui

AU - Tank, Marcus

AU - Ferlez, Bryan H.

AU - Canniffe, Daniel P.

AU - Lahav, Yigal

AU - Bellstedt, Peter

AU - Alia, A.

AU - Schapiro, Igor

AU - Golbeck, John H.

AU - Bryant, Donald A.

AU - Matysik, Jörg

N1 - Funding Information: 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). Funding Information: The authors thank Dr. Matthias Findeisen for technical assistence, Eva-Maria H?hn (Group of Professor Dr. Detlev Belder, Universit?t 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). Publisher Copyright: © 2018, Springer Science+Business Media B.V., part of Springer Nature.

PY - 2018/8/1

Y1 - 2018/8/1

N2 - 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.

AB - 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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KW - Photo-CIDNP

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