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Chemical compass model of avian magnetoreception

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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Figure 1: C–P–F triad.
Figure 2: Isotropic magnetic field effects on C–P–F.
Figure 3: Operation of C–P–F as a chemical compass.

References

  1. Johnsen, S. & Lohmann, K. J. The physics and neurobiology of magnetoreception. Nature Rev. Neurosci. 6, 703–712 (2005)

    Article  CAS  Google Scholar 

  2. Schulten, K., Swenberg, C. E. & Weller, A. A biomagnetic sensory mechanism based on magnetic field modulated coherent electron spin motion. Z. Phys. Chem. NF111, 1–5 (1978)

    Article  Google Scholar 

  3. Ritz, T., Adem, S. & Schulten, K. A model for photoreceptor-based magnetoreception in birds. Biophys. J. 78, 707–718 (2000)

    Article  CAS  Google Scholar 

  4. Ritz, T., Thalau, P., Phillips, J. B., Wiltschko, R. & Wiltschko, W. Resonance effects indicate a radical-pair mechanism for avian magnetic compass. Nature 429, 177–180 (2004)

    Article  ADS  CAS  Google Scholar 

  5. Möller, A., Sagasser, S., Wiltschko, W. & Schierwater, B. Retinal cryptochrome in a migratory passerine bird: A possible transducer for the avian magnetic compass. Naturwissenschaften 91, 585–588 (2004)

    Article  ADS  Google Scholar 

  6. Mouritsen, H. 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)

    Article  ADS  CAS  Google Scholar 

  7. Weaver, J. C., Vaughan, T. E. & Astumian, R. D. Biological sensing of small field differences by magnetically sensitive chemical reactions. Nature 405, 707–709 (2000)

    Article  ADS  CAS  Google Scholar 

  8. Cintolesi, F., Ritz, T., Kay, C. W. M., Timmel, C. R. & Hore, P. J. Anisotropic recombination of an immobilized photoinduced radical pair in a 50-μT magnetic field: A model avian photomagnetoreceptor. Chem. Phys. 294, 385–399 (2003)

    Article  CAS  Google Scholar 

  9. Wang, K., Mattern, E. & Ritz, T. On the use of magnets to disrupt the physiological compass of birds. Phys. Biol. 3, 220–231 (2006)

    Article  ADS  CAS  Google Scholar 

  10. Solov'yov, I. A., Chandler, D. E. & Schulten, K. Magnetic field effects in Arabidopsis thaliana cryptochrome-1. Biophys. J. 92, 2711–2726 (2007)

    Article  ADS  CAS  Google Scholar 

  11. Ahmad, M., Galland, P., Ritz, T., Wiltschko, R. & Wiltschko, W. Magnetic intensity affects cryptochrome-dependent responses in Arabidopsis thaliana. Planta 225, 615–624 (2007)

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  14. Wiltschko, W. & Wiltschko, R. 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)

    CAS  PubMed  MATH  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  16. Rodgers, C. T., Henbest, K. B., Kukura, P., Timmel, C. R. & Hore, P. J. Low-field optically detected EPR spectroscopy of transient photoinduced radical pairs. J. Phys. Chem. A 109, 5035–5041 (2005)

    Article  CAS  Google Scholar 

  17. Thalau, P., Ritz, T., Stapput, K., Wiltschko, R. & Wiltschko, W. Magnetic compass orientation of migratory birds in the presence of a 1.315 MHz oscillating field. Naturwissenschaften 92, 86–90 (2005)

    Article  ADS  CAS  Google Scholar 

  18. Kodis, G., Liddell, P. A., Moore, A. L., Moore, T. A. & Gust, D. Synthesis and photochemistry of a carotene-porphyrin-fullerene model photosynthetic reaction center. J. Phys. Org. Chem. 17, 724–734 (2004)

    Article  CAS  Google Scholar 

  19. Kuciauskas, D., Liddell, P. A., Moore, A. L., Moore, T. A. & Gust, D. Magnetic switching of charge separation lifetimes in artificial photosynthetic reaction centers. J. Am. Chem. Soc. 120, 10880–10886 (1998)

    Article  CAS  Google Scholar 

  20. Liddell, P. A. 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)

    Article  CAS  Google Scholar 

  21. van Dijk, B., Carpenter, J. K. H., Hoff, A. J. & Hore, P. J. Magnetic field effects on the recombination kinetics of radical pairs. J. Phys. Chem. B 102, 464–472 (1998)

    Article  CAS  Google Scholar 

  22. Timmel, C. R., Till, U., Brocklehurst, B., McLauchlan, K. A. & Hore, P. J. Effects of weak magnetic fields on free radical recombination reactions. Mol. Phys. 95, 71–89 (1998)

    Article  ADS  CAS  Google Scholar 

  23. Rodgers, C. T., Norman, S. A., Henbest, K. B., Timmel, C. R. & Hore, P. J. Determination of radical re-encounter probability distributions from magnetic field effects on reaction yields. J. Am. Chem. Soc. 129, 6746–6755 (2007)

    Article  CAS  Google Scholar 

  24. Poluektov, O. G., Paschenko, S. V., Utschig, L. M., Lakshmi, K. V. & Thurnauer, M. C. Bidirectional electron transfer in Photosystem I: Direct evidence from high-frequency time-resolved EPR spectroscopy. J. Am. Chem. Soc. 127, 11910–11911 (2005)

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  27. Prabhakar, R., Siegbahn, P. E. M., Minaev, B. F. & Agren, H. Activation of triplet dioxygen by glucose oxidase: spin-orbit coupling in the superoxide ion. J. Phys. Chem. B 106, 3742–3750 (2002)

    Article  CAS  Google Scholar 

  28. Henbest, K. B., Kukura, P., Rodgers, C. T., Hore, P. J. & Timmel, C. R. 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)

    Article  CAS  Google Scholar 

  29. Buchachenko, A. L., Kouznetsov, D. A., Orlova, M. A. & Markarian, A. A. Magnetic isotope effect of magnesium in phosphoglycerate kinase phosphorylation. Proc. Natl Acad. Sci. USA 102, 10793–10796 (2005)

    Article  ADS  CAS  Google Scholar 

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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.

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

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Maeda, K., Henbest, K., Cintolesi, F. et al. Chemical compass model of avian magnetoreception. Nature 453, 387–390 (2008). https://doi.org/10.1038/nature06834

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