TY - JOUR

T1 - Tailored flavoproteins acting as light-driven spin machines pump nuclear hyperpolarization

AU - Ding, Yonghong

AU - Kiryutin, Alexey S.

AU - Zhao, Ziyue

AU - Xu, Qian Zhao

AU - Zhao, Kai Hong

AU - Kurle, Patrick

AU - Bannister, Saskia

AU - Kottke, Tilman

AU - Sagdeev, Renad Z.

AU - Ivanov, Konstantin L.

AU - Yurkovskaya, Alexandra V.

AU - Matysik, Jörg

PY - 2020/12/1

Y1 - 2020/12/1

N2 - The solid-state photo-chemically induced dynamic nuclear polarization (photo-CIDNP) effect generates non-Boltzmann nuclear spin magnetization, referred to as hyperpolarization, allowing for high gain of sensitivity in nuclear magnetic resonance (NMR). Well known to occur in photosynthetic reaction centers, the effect was also observed in a light-oxygen-voltage (LOV) domain of the blue-light receptor phototropin, in which the functional cysteine was removed to prevent photo-chemical reactions with the cofactor, a flavin mononucleotide (FMN). Upon illumination, the FMN abstracts an electron from a tryptophan to form a transient spin-correlated radical pair (SCRP) generating the photo-CIDNP effect. Here, we report on designed molecular spin-machines producing nuclear hyperpolarization upon illumination: a LOV domain of aureochrome1a from Phaeodactylum tricornutum, and a LOV domain named 4511 from Methylobacterium radiotolerans (Mr4511) which lacks an otherwise conserved tryptophan in its wild-type form. Insertion of the tryptophan at canonical and novel positions in Mr4511 yields photo-CIDNP effects observed by 15N and 1H liquid-state high-resolution NMR with a characteristic magnetic-field dependence indicating an involvement of anisotropic magnetic interactions and a slow-motion regime in the transient paramagnetic state. The heuristic biomimetic design opens new categories of experiments to analyze and apply the photo-CIDNP effect.

AB - The solid-state photo-chemically induced dynamic nuclear polarization (photo-CIDNP) effect generates non-Boltzmann nuclear spin magnetization, referred to as hyperpolarization, allowing for high gain of sensitivity in nuclear magnetic resonance (NMR). Well known to occur in photosynthetic reaction centers, the effect was also observed in a light-oxygen-voltage (LOV) domain of the blue-light receptor phototropin, in which the functional cysteine was removed to prevent photo-chemical reactions with the cofactor, a flavin mononucleotide (FMN). Upon illumination, the FMN abstracts an electron from a tryptophan to form a transient spin-correlated radical pair (SCRP) generating the photo-CIDNP effect. Here, we report on designed molecular spin-machines producing nuclear hyperpolarization upon illumination: a LOV domain of aureochrome1a from Phaeodactylum tricornutum, and a LOV domain named 4511 from Methylobacterium radiotolerans (Mr4511) which lacks an otherwise conserved tryptophan in its wild-type form. Insertion of the tryptophan at canonical and novel positions in Mr4511 yields photo-CIDNP effects observed by 15N and 1H liquid-state high-resolution NMR with a characteristic magnetic-field dependence indicating an involvement of anisotropic magnetic interactions and a slow-motion regime in the transient paramagnetic state. The heuristic biomimetic design opens new categories of experiments to analyze and apply the photo-CIDNP effect.

KW - ELECTRON-PARAMAGNETIC-RESONANCE

KW - PHOTOSYNTHETIC REACTION CENTERS

KW - SOLID-STATE NMR

KW - CIDNP MAS NMR

KW - LOV2 DOMAIN

KW - MOLECULAR-MECHANISM

KW - CRYSTAL-STRUCTURES

KW - PHOTOSYSTEM-II

KW - RADICAL PAIRS

KW - POLARIZATION

UR - http://www.scopus.com/inward/record.url?scp=85094216212&partnerID=8YFLogxK

U2 - 10.1038/s41598-020-75627-z

DO - 10.1038/s41598-020-75627-z

M3 - Article

C2 - 33122681

AN - SCOPUS:85094216212

VL - 10

JO - Scientific Reports

JF - Scientific Reports

SN - 2045-2322

IS - 1

M1 - 18658

ER -