Magnetic resonance control of spin-correlated radical pair dynamics in vivo | Nature
Subjects
- Biological fluorescence
- Biomedical engineering
- Quantum physics
Abstract
Magnetic fields can influence reactions involving spin-correlated radical pairs (SCRPs)1,2. This provides a mechanism by which both static and time-varying magnetic fields can affect living systems at the biomolecular level3. However, an engineered SCRP system conferring magnetic sensitivity to a non-native biochemical process in a multicellular organism has not yet been demonstrated. Here we demonstrate control of SCRP dynamics using magnetic resonance in a live transgenic animal. We show that the emission of various red fluorescent proteins (RFPs), in the presence of a flavin cofactor, can be modified by a combination of static and radiofrequency magnetic fields applied near the electron spin resonance frequency. This effect was measured at room temperature both in vitro and in the nematode Caenorhabditis elegans, genetically modified to express the RFP mScarlet4. These observations suggest that the magnetic field effects measured in RFP-flavin systems5 are due to quantum-correlated radical pairs with a coherence time larger than 4 ns. Our experiments demonstrate that radiofrequency magnetic fields can influence dynamics of reactions involving SCRPs in vivo, potentially enabling new methods for remotely controlling biomolecular processes, such as gene expression, and suggest broader potential for quantum tools in biology.
Access through your institution
Buy or subscribe
This is a preview of subscription content, access via your institution
Access options
Access through your institution
Access Nature and 54 other Nature Portfolio journals
Get Nature+, our best-value online-access subscription
$32.99 / 30 days
cancel any time
Learn more
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Learn more
Buy this article
- Purchase on SpringerLink
- Instant access to the full article PDF.
USD 39.95
Prices may be subject to local taxes which are calculated during checkout
Fig. 1: Modulation of fluorescence from RFPs in a fluorescent protein: flavin system using RF magnetic fields.
Fig. 2: RYDMR from an aqueous solution of purified mScarlet-I and FMN.
Fig. 3: Electron spin resonance.
Fig. 4: MFEs and RYDMR in C. elegans expressing mScarlet.
Data availability
The raw data supporting this study are available at Zenodo36 (https://doi.org/10.5281/zenodo.15321800). The crystal structure of RFP mScarlet is available from the Protein Data Bank (PDB ID 5LK4; https://doi.org/10.2210/pdb5lk4/pdb).
Code availability
The custom codes used to analyse the data in this study are available at Zenodo36 (https://doi.org/10.5281/zenodo.15321800).
References
- Kaptein, R. & Oosterhoff, J. L. Chemically induced dynamic nuclear polarization II: (relationwith anomalous ESR spectra). Chem. Phys. Lett. 4, 195–197 (1969).
Article
ADS
CAS
Google Scholar
- Closs, G. L. Mechanism explaining nuclear spin polarizations in radical combination reactions. J. Am. Chem. Soc. 91, 4552–4554 (1969).
Article
ADS
CAS
Google Scholar
- Hore, P. J. & Mouritsen, H. The radical-pair mechanism of magnetoreception. Annu. Rev. Biophys. 45, 299–344 (2016).
Article
CAS
PubMed
Google Scholar
- Bindels, D. S. et al. mScarlet: a bright monomeric red fluorescent protein for cellular imaging. Nat. Methods 14, 53–56 (2017).
Article
CAS
PubMed
Google Scholar
- Hayward, R. F. et al. Magnetic control of the brightness of fluorescent proteins. Zenodo https://doi.org/10.5281/zenodo.8137174 (2024).
- Kubarev, S. J. & Pshenichnov, E. A. The effect of high frequency magnetic fields on the recombination of radicals. Chem. Phys. Lett. 28, 66–67 (1974).
Article
ADS
CAS
Google Scholar
- Anisimov, O. A., Grigoryants, V. M., Molchanov, V. K. & Molin, Y. N. Optical detection of ESR absorption of short-lived ion-radical pairs produced in solution by ionizing radiation. Chem. Phys. Lett. 66, 265–268 (1979).
Article
ADS
CAS
Google Scholar
- Steiner, U. E. & Ulrich, T. Magnetic field effects in chemical kinetics and related phenomena. Chem. Rev. 89, 51–147 (1989).
Article
CAS
Google Scholar
- Hoff, A. J. Magnetic field effects on photosynthetic reactions. Q. Rev. Biophys. 14, 599–665 (1981).
Article
CAS
PubMed
Google Scholar
- Boxer, S. G., Chidsey, C. E. D. & Roelofs, M. G. Magnetic field effects on reaction yields in the solid state: an example from photosynthetic reaction centers. Annu. Rev. Phys. Chem. 34, 389–417 (1983).
Article
ADS
CAS
Google Scholar
- Miura, T., Maeda, K. & Arai, T. Effect of Coulomb interaction on the dynamics of the radical pair in the system of flavin mononucleotide and hen egg-white lysozyme (HEWL) studied by a magnetic field effect. J. Phys. Chem. B 107, 6474–6478 (2003).
Article
CAS
Google Scholar
- Evans, E. W. et al. Sensitive fluorescence-based detection of magnetic field effects in photoreactions of flavins. Phys. Chem. Chem. Phys. 17,