Letter | Published:

Chemical compass model of avian magnetoreception

Nature volume 453, pages 387390 (15 May 2008) | Download Citation

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Abstract

Approximately 50 species, including birds, mammals, reptiles, amphibians, fish, crustaceans and insects, are known to use the Earth’s magnetic field for orientation and navigation1. Birds in particular have been intensively studied, but the biophysical mechanisms that underlie the avian magnetic compass are still poorly understood. One proposal, based on magnetically sensitive free radical reactions2,3, is gaining support4,5,6,7,8,9,10,11 despite the fact that no chemical reaction in vitro has been shown to respond to magnetic fields as weak as the Earth’s (50 μT) or to be sensitive to the direction of such a field. Here we use spectroscopic observation of a carotenoid–porphyrin–fullerene model system to demonstrate that the lifetime of a photochemically formed radical pair is changed by application of ≤50 μT magnetic fields, and to measure the anisotropic chemical response that is essential for its operation as a chemical compass sensor. These experiments establish the feasibility of chemical magnetoreception and give insight into the structural and dynamic design features required for optimal detection of the direction of the Earth’s magnetic field.

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References

  1. 1.

    & The physics and neurobiology of magnetoreception. Nature Rev. Neurosci. 6, 703–712 (2005)

  2. 2.

    , & A biomagnetic sensory mechanism based on magnetic field modulated coherent electron spin motion. Z. Phys. Chem. NF111, 1–5 (1978)

  3. 3.

    , & A model for photoreceptor-based magnetoreception in birds. Biophys. J. 78, 707–718 (2000)

  4. 4.

    , , , & Resonance effects indicate a radical-pair mechanism for avian magnetic compass. Nature 429, 177–180 (2004)

  5. 5.

    , , & Retinal cryptochrome in a migratory passerine bird: A possible transducer for the avian magnetic compass. Naturwissenschaften 91, 585–588 (2004)

  6. 6.

    et al. Cryptochromes and neuronal-activity markers colocalize in the retina of migratory birds during magnetic orientation. Proc. Natl Acad. Sci. USA 101, 14294–14299 (2004)

  7. 7.

    , & Biological sensing of small field differences by magnetically sensitive chemical reactions. Nature 405, 707–709 (2000)

  8. 8.

    , , , & Anisotropic recombination of an immobilized photoinduced radical pair in a 50-μT magnetic field: A model avian photomagnetoreceptor. Chem. Phys. 294, 385–399 (2003)

  9. 9.

    , & On the use of magnets to disrupt the physiological compass of birds. Phys. Biol. 3, 220–231 (2006)

  10. 10.

    , & Magnetic field effects in Arabidopsis thaliana cryptochrome-1. Biophys. J. 92, 2711–2726 (2007)

  11. 11.

    , , , & Magnetic intensity affects cryptochrome-dependent responses in Arabidopsis thaliana. Planta 225, 615–624 (2007)

  12. 12.

    Magnetic fields and radical reactions: Recent developments and their role in nature. Chem. Soc. Rev. 31, 301–311 (2002)

  13. 13.

    & A study of spin chemistry in weak magnetic fields. Phil. Trans. R. Soc. Lond. A 362, 2573–2589 (2004)

  14. 14.

    & Light-dependent magnetoreception in birds: The behaviour of European robins, Erithacus rubecula, under monochromatic light of various wavelengths and intensities. J. Exp. Biol. 204, 3295–3302 (2001)

  15. 15.

    & Magnetic compass of European robins. Science 176, 62–64 (1972)

  16. 16.

    , , , & Low-field optically detected EPR spectroscopy of transient photoinduced radical pairs. J. Phys. Chem. A 109, 5035–5041 (2005)

  17. 17.

    , , , & Magnetic compass orientation of migratory birds in the presence of a 1.315 MHz oscillating field. Naturwissenschaften 92, 86–90 (2005)

  18. 18.

    , , , & Synthesis and photochemistry of a carotene-porphyrin-fullerene model photosynthetic reaction center. J. Phys. Org. Chem. 17, 724–734 (2004)

  19. 19.

    , , , & Magnetic switching of charge separation lifetimes in artificial photosynthetic reaction centers. J. Am. Chem. Soc. 120, 10880–10886 (1998)

  20. 20.

    et al. Photoinduced charge separation and charge recombination to a triplet state in a carotene-porphyrin-fullerene triad. J. Am. Chem. Soc. 119, 1400–1405 (1997)

  21. 21.

    , , & Magnetic field effects on the recombination kinetics of radical pairs. J. Phys. Chem. B 102, 464–472 (1998)

  22. 22.

    , , , & Effects of weak magnetic fields on free radical recombination reactions. Mol. Phys. 95, 71–89 (1998)

  23. 23.

    , , , & Determination of radical re-encounter probability distributions from magnetic field effects on reaction yields. J. Am. Chem. Soc. 129, 6746–6755 (2007)

  24. 24.

    , , , & Bidirectional electron transfer in Photosystem I: Direct evidence from high-frequency time-resolved EPR spectroscopy. J. Am. Chem. Soc. 127, 11910–11911 (2005)

  25. 25.

    & The role of exchange and dipolar interactions in the radical pair model of the avian magnetic compass. Biophys. J. 94, 1565–1574 (2008)

  26. 26.

    Light-driven enzymatic catalysis of DNA repair: A review of recent biophysical studies on photolyase. Biochim. Biophys. Acta 1707, 1–23 (2005)

  27. 27.

    , , & Activation of triplet dioxygen by glucose oxidase: spin-orbit coupling in the superoxide ion. J. Phys. Chem. B 106, 3742–3750 (2002)

  28. 28.

    , , , & Radio frequency magnetic field effects on a radical recombination reaction: A diagnostic test for the radical pair mechanism. J. Am. Chem. Soc. 126, 8102–8103 (2004)

  29. 29.

    , , & Magnetic isotope effect of magnesium in phosphoglycerate kinase phosphorylation. Proc. Natl Acad. Sci. USA 102, 10793–10796 (2005)

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Acknowledgements

We thank M. Ahmad, D. Carbonera, M. di Valentin, G. Giacometti, C. W. M. Kay, P. Raynes, T. Ritz and R. Wiltschko for discussions; N. Baker for technical assistance; and the Oxford Supercomputing Centre for allocation of CPU time. P.J.H., C.R.T. and co-workers are funded by the Engineering and Physical Sciences Research Council, the Human Frontier Science Program, the EMF Biological Research Trust and the Royal Society. D.G. and co-workers are funded by the US National Science Foundation. I.K. is a Fellow by Examination at Magdalen College, Oxford.

Author Contributions K.M., K.B.H. and F.C. performed the experiments. K.M., K.B.H. and C.R.T analysed the data. P.A.L. and D.G. synthesized the triad molecule. C.T.R. and P.J.H. analysed the orientational averaging. I.K. performed ab initio calculations. F.C., C.R.T. and P.J.H. designed the study. C.R.T. co-ordinated the study. P.J.H. wrote the paper. All authors discussed the results and commented on the manuscript.

Author information

Author notes

    • Kiminori Maeda
    •  & Kevin B. Henbest

    These authors contributed equally to this work.

Affiliations

  1. Department of Chemistry, University of Oxford, Inorganic Chemistry Laboratory, South Parks Road, Oxford OX1 3QR, UK

    • Kiminori Maeda
    • , Kevin B. Henbest
    •  & Christiane R. Timmel
  2. Department of Chemistry, University of Oxford, Physical and Theoretical Chemistry Laboratory, South Parks Road, Oxford OX1 3QZ, UK

    • Filippo Cintolesi
    • , Ilya Kuprov
    • , Christopher T. Rodgers
    •  & P. J. Hore
  3. Department of Chemistry and Biochemistry, Arizona State University, Tempe, Arizona 85287, USA

    • Paul A. Liddell
    •  & Devens Gust

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Correspondence to Christiane R. Timmel or P. J. Hore.

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DOI

https://doi.org/10.1038/nature06834

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