Nuclear spin-hyperpolarization generated in a flavoprotein under illumination: experimental field-dependence and theoretical level crossing analysis

Yonghong Ding; Alexey S. Kiryutin; Alexandra V. Yurkovskaya; Denis V. Sosnovsky; Renad Z. Sagdeev; Saskia Bannister; Tilman Kottke; Rajiv K. Kar; Igor Schapiro; Konstantin L. Ivanov; Jörg Matysik

doi:10.1038/s41598-019-54671-4

Nuclear spin-hyperpolarization generated in a flavoprotein under illumination: experimental field-dependence and theoretical level crossing analysis

Yonghong Ding, Alexey S. Kiryutin, Alexandra V. Yurkovskaya, Denis V. Sosnovsky, Renad Z. Sagdeev, Saskia Bannister, Tilman Kottke, Rajiv K. Kar, Igor Schapiro, Konstantin L. Ivanov, Jörg Matysik^*

^*Corresponding author for this work

Institute of Chemistry

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

15 Scopus citations

Abstract

The solid-state photo-chemically induced dynamic nuclear polarization (photo-CIDNP) effect generates non-equilibrium nuclear spin polarization in frozen electron-transfer proteins upon illumination and radical-pair formation. The effect can be observed in various natural photosynthetic reaction center proteins using magic-angle spinning (MAS) nuclear magnetic resonance (NMR) spectroscopy, and in a flavin-binding light-oxygen-voltage (LOV) domain of the blue-light receptor phototropin. In the latter system, a functionally instrumental cysteine has been mutated to interrupt the natural cysteine-involving photochemistry allowing for an electron transfer from a more distant tryptophan to the excited flavin mononucleotide chromophore. We explored the solid-state photo-CIDNP effect and its mechanisms in phototropin-LOV1-C57S from the green alga Chlamydomonas reinhardtii by using field-cycling solution NMR. We observed the ¹³C and, to our knowledge, for the first time, ¹⁵N photo-CIDNP signals from phototropin-LOV1-C57S. Additionally, the ¹H photo-CIDNP signals of residual water in the deuterated buffer of the protein were detected. The relative strengths of the photo-CIDNP effect from the three types of nuclei, ¹H, ¹³C and ¹⁵N were measured in dependence of the magnetic field, showing their maximum polarizations at different magnetic fields. Theoretical level crossing analysis demonstrates that anisotropic mechanisms play the dominant role at high magnetic fields.

Original language	American English
Article number	18436
Journal	Scientific Reports
Volume	9
Issue number	1
DOIs	https://doi.org/10.1038/s41598-019-54671-4
State	Published - 1 Dec 2019

Bibliographical note

Funding Information:
Y.D. acknowledges the Russian Foundation of Basic Research (Grant No. 19-33-50094) and the Deutscher Akademischer Austauschdienst (Referat ST22) for supporting his work in Novosibirsk. A.S.K., A.V.Y., D.V.S., R.Z.S. and K.L.I. acknowledge the Russian Foundation of Basic Research (Grant No. 17-03-00932) and the Russian Ministry for Science and Higher Education (Project No. AAAA-A16-116121510087-5). J.M. thanks the Deutsche Forschungsgemeinschaft (MA 4972/11-1). I.S. acknowledges funding by the European Research Council (ERC) under European Union’s Horizon 2020 research and innovation program (grant agreement 678169 “Photomutant”). R.K.K. thanks the Lady Davis Trust for a Shunbrun postdoctoral fellowship. T.K. acknowledges support by a Heisenberg fellowship of the Deutsche Forschungsgemeinschaft (KO 3580/4-2).

Publisher Copyright:
© 2019, The Author(s).

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Ding, Y., Kiryutin, A. S., Yurkovskaya, A. V., Sosnovsky, D. V., Sagdeev, R. Z., Bannister, S., Kottke, T., Kar, R. K., Schapiro, I., Ivanov, K. L., & Matysik, J. (2019). Nuclear spin-hyperpolarization generated in a flavoprotein under illumination: experimental field-dependence and theoretical level crossing analysis. Scientific Reports, 9(1), Article 18436. https://doi.org/10.1038/s41598-019-54671-4

@article{86802f8c0cf74eccbf96cd4d2ef184f5,

title = "Nuclear spin-hyperpolarization generated in a flavoprotein under illumination: experimental field-dependence and theoretical level crossing analysis",

abstract = "The solid-state photo-chemically induced dynamic nuclear polarization (photo-CIDNP) effect generates non-equilibrium nuclear spin polarization in frozen electron-transfer proteins upon illumination and radical-pair formation. The effect can be observed in various natural photosynthetic reaction center proteins using magic-angle spinning (MAS) nuclear magnetic resonance (NMR) spectroscopy, and in a flavin-binding light-oxygen-voltage (LOV) domain of the blue-light receptor phototropin. In the latter system, a functionally instrumental cysteine has been mutated to interrupt the natural cysteine-involving photochemistry allowing for an electron transfer from a more distant tryptophan to the excited flavin mononucleotide chromophore. We explored the solid-state photo-CIDNP effect and its mechanisms in phototropin-LOV1-C57S from the green alga Chlamydomonas reinhardtii by using field-cycling solution NMR. We observed the 13C and, to our knowledge, for the first time, 15N photo-CIDNP signals from phototropin-LOV1-C57S. Additionally, the 1H photo-CIDNP signals of residual water in the deuterated buffer of the protein were detected. The relative strengths of the photo-CIDNP effect from the three types of nuclei, 1H, 13C and 15N were measured in dependence of the magnetic field, showing their maximum polarizations at different magnetic fields. Theoretical level crossing analysis demonstrates that anisotropic mechanisms play the dominant role at high magnetic fields.",

author = "Yonghong Ding and Kiryutin, {Alexey S.} and Yurkovskaya, {Alexandra V.} and Sosnovsky, {Denis V.} and Sagdeev, {Renad Z.} and Saskia Bannister and Tilman Kottke and Kar, {Rajiv K.} and Igor Schapiro and Ivanov, {Konstantin L.} and J{\"o}rg Matysik",

note = "Funding Information: Y.D. acknowledges the Russian Foundation of Basic Research (Grant No. 19-33-50094) and the Deutscher Akademischer Austauschdienst (Referat ST22) for supporting his work in Novosibirsk. A.S.K., A.V.Y., D.V.S., R.Z.S. and K.L.I. acknowledge the Russian Foundation of Basic Research (Grant No. 17-03-00932) and the Russian Ministry for Science and Higher Education (Project No. AAAA-A16-116121510087-5). J.M. thanks the Deutsche Forschungsgemeinschaft (MA 4972/11-1). I.S. acknowledges funding by the European Research Council (ERC) under European Union{\textquoteright}s Horizon 2020 research and innovation program (grant agreement 678169 “Photomutant”). R.K.K. thanks the Lady Davis Trust for a Shunbrun postdoctoral fellowship. T.K. acknowledges support by a Heisenberg fellowship of the Deutsche Forschungsgemeinschaft (KO 3580/4-2). Publisher Copyright: {\textcopyright} 2019, The Author(s).",

year = "2019",

month = dec,

day = "1",

doi = "10.1038/s41598-019-54671-4",

language = "American English",

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journal = "Scientific Reports",

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Ding, Y, Kiryutin, AS, Yurkovskaya, AV, Sosnovsky, DV, Sagdeev, RZ, Bannister, S, Kottke, T, Kar, RK, Schapiro, I, Ivanov, KL & Matysik, J 2019, 'Nuclear spin-hyperpolarization generated in a flavoprotein under illumination: experimental field-dependence and theoretical level crossing analysis', Scientific Reports, vol. 9, no. 1, 18436. https://doi.org/10.1038/s41598-019-54671-4

TY - JOUR

T1 - Nuclear spin-hyperpolarization generated in a flavoprotein under illumination

T2 - experimental field-dependence and theoretical level crossing analysis

AU - Ding, Yonghong

AU - Kiryutin, Alexey S.

AU - Yurkovskaya, Alexandra V.

AU - Sosnovsky, Denis V.

AU - Sagdeev, Renad Z.

AU - Bannister, Saskia

AU - Kottke, Tilman

AU - Kar, Rajiv K.

AU - Schapiro, Igor

AU - Ivanov, Konstantin L.

AU - Matysik, Jörg

N1 - Funding Information: Y.D. acknowledges the Russian Foundation of Basic Research (Grant No. 19-33-50094) and the Deutscher Akademischer Austauschdienst (Referat ST22) for supporting his work in Novosibirsk. A.S.K., A.V.Y., D.V.S., R.Z.S. and K.L.I. acknowledge the Russian Foundation of Basic Research (Grant No. 17-03-00932) and the Russian Ministry for Science and Higher Education (Project No. AAAA-A16-116121510087-5). J.M. thanks the Deutsche Forschungsgemeinschaft (MA 4972/11-1). I.S. acknowledges funding by the European Research Council (ERC) under European Union’s Horizon 2020 research and innovation program (grant agreement 678169 “Photomutant”). R.K.K. thanks the Lady Davis Trust for a Shunbrun postdoctoral fellowship. T.K. acknowledges support by a Heisenberg fellowship of the Deutsche Forschungsgemeinschaft (KO 3580/4-2). Publisher Copyright: © 2019, The Author(s).

PY - 2019/12/1

Y1 - 2019/12/1

N2 - The solid-state photo-chemically induced dynamic nuclear polarization (photo-CIDNP) effect generates non-equilibrium nuclear spin polarization in frozen electron-transfer proteins upon illumination and radical-pair formation. The effect can be observed in various natural photosynthetic reaction center proteins using magic-angle spinning (MAS) nuclear magnetic resonance (NMR) spectroscopy, and in a flavin-binding light-oxygen-voltage (LOV) domain of the blue-light receptor phototropin. In the latter system, a functionally instrumental cysteine has been mutated to interrupt the natural cysteine-involving photochemistry allowing for an electron transfer from a more distant tryptophan to the excited flavin mononucleotide chromophore. We explored the solid-state photo-CIDNP effect and its mechanisms in phototropin-LOV1-C57S from the green alga Chlamydomonas reinhardtii by using field-cycling solution NMR. We observed the 13C and, to our knowledge, for the first time, 15N photo-CIDNP signals from phototropin-LOV1-C57S. Additionally, the 1H photo-CIDNP signals of residual water in the deuterated buffer of the protein were detected. The relative strengths of the photo-CIDNP effect from the three types of nuclei, 1H, 13C and 15N were measured in dependence of the magnetic field, showing their maximum polarizations at different magnetic fields. Theoretical level crossing analysis demonstrates that anisotropic mechanisms play the dominant role at high magnetic fields.

AB - The solid-state photo-chemically induced dynamic nuclear polarization (photo-CIDNP) effect generates non-equilibrium nuclear spin polarization in frozen electron-transfer proteins upon illumination and radical-pair formation. The effect can be observed in various natural photosynthetic reaction center proteins using magic-angle spinning (MAS) nuclear magnetic resonance (NMR) spectroscopy, and in a flavin-binding light-oxygen-voltage (LOV) domain of the blue-light receptor phototropin. In the latter system, a functionally instrumental cysteine has been mutated to interrupt the natural cysteine-involving photochemistry allowing for an electron transfer from a more distant tryptophan to the excited flavin mononucleotide chromophore. We explored the solid-state photo-CIDNP effect and its mechanisms in phototropin-LOV1-C57S from the green alga Chlamydomonas reinhardtii by using field-cycling solution NMR. We observed the 13C and, to our knowledge, for the first time, 15N photo-CIDNP signals from phototropin-LOV1-C57S. Additionally, the 1H photo-CIDNP signals of residual water in the deuterated buffer of the protein were detected. The relative strengths of the photo-CIDNP effect from the three types of nuclei, 1H, 13C and 15N were measured in dependence of the magnetic field, showing their maximum polarizations at different magnetic fields. Theoretical level crossing analysis demonstrates that anisotropic mechanisms play the dominant role at high magnetic fields.

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U2 - 10.1038/s41598-019-54671-4

DO - 10.1038/s41598-019-54671-4

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VL - 9

JO - Scientific Reports

JF - Scientific Reports

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M1 - 18436

ER -

Nuclear spin-hyperpolarization generated in a flavoprotein under illumination: experimental field-dependence and theoretical level crossing analysis

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