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Chemical Magnetoreception in Birds: the Radical Pair Mechanism

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Chemical Magnetoreception in Birds: the Radical Pair Mechanism PERSPECTIVE Chemical magnetoreception in birds: The radical pair mechanism Christopher T. Rodgersa,b and P. J. Horea,1 aDepartment of Chemistry, Physical and Theoretical Chemistry Laboratory, University of Oxford, South Parks Road, Oxford, OX1 3QZ, United Kingdom; and bOxford Centre for Clinical Magnetic Resonance Research, Level 0, John Radcliffe Hospital, Oxford, OX3 9DU, United Kingdom Edited by Nicholas J. Turro, Columbia University, New York, NY, and approved December 2, 2008 (received for review September 24, 2008) Migratory birds travel vast distances each year, finding their way by various means, including a remarkable ability to perceive the Earth’s magnetic field. Although it has been known for 40 years that birds possess a magnetic compass, avian magnetoreception is poorly understood at all levels from the primary biophysical detection events, signal transduction pathways and neurophysiology, to the processing of information in the brain. It has been proposed that the primary detector is a specialized ocular photoreceptor that plays host to magnetically sensitive photochemical reactions having radical pairs as fleeting intermediates. Here, we present a physi- cal chemist’s perspective on the ‘‘radical pair mechanism’’ of compass magnetoreception in birds. We outline the essential chemical requirements for detecting the direction of an Earth-strength Ϸ50 ␮T magnetic field and comment on the likelihood that these might be satisfied in a biologically plausible receptor. Our survey concludes with a discussion of cryptochrome, the photoactive protein that has been put forward as the magnetoreceptor molecule. ould a chemical reaction be The radical pair mechanism [and a pair model, or to comment on (neuro)- used to detect the direction of few rare variants (10)] is currently the physiological aspects of magnetorecep- the Earth’s magnetic field? At only plausible way in which weak mag- tion, all of which have been covered first sight, most physical chem- netic fields can affect chemical reactiv- authoritatively and extensively in recent Cists would be skeptical. The energy of ity. Most experimental studies have reviews (3–5, 8, 24, 25). Nor do we pre- interaction of a molecule with a Ϸ50-␮T been of photochemically formed organic sume here to debate the relative merits magnetic field is Ͼ6 orders of magni- radicals in solution. The effects are usu- of the radical pair hypothesis versus pro- tude smaller than the average thermal ally not dramatic—typically Ͻ50% posals based on biogenic magnetite energy kBT, which in turn is 10–100 change in reaction yields or radical life- (Fe3O4) (26–32). We close with a dis- times smaller than the strength of a times and, with few exceptions (14), are cussion of cryptochrome, the photore- chemical bond. It therefore seems in- observed for magnetic field intensities ceptor protein that is presently the only conceivable that the position of a (1 mT–10 T) considerably stronger than molecule under consideration as the chemical equilibrium or the rate of an the Earth’s (25–65 ␮T). Compared with magnetoreceptor (2), and make sugges- activated chemical reaction could be these chemical studies, there are rela- tions for further research. We hope that significantly altered by such a minuscule tively few reliable examples of magnetic the thoughts set out here will be of in- perturbation. Nevertheless, there is field effects on biological processes, the terest to both physical and biological growing evidence that the striking abil- most notable by far being photosynthetic scientists who may be inspired to con- ity of birds to detect the direction of the reaction center proteins where light ab- tribute to the elucidation of this intrigu- geomagnetic field (1) is based on a sorption leads to radical pair formation ing and incompletely understood chemical reaction whose product yields by sequential electron transfer steps sensory mechanism. depend on the orientation of the reac- (reviewed in refs. 15–17). tants within the field (2) (for reviews, Radical pair reactions were first pro- Key Features of a Radical Pair see also refs. 3–8). posed as a magnetoreceptor by Schulten Magnetoreceptor It has been known since the 1970s (18, 19), prompted by the findings that Chemistry. Magnetically sensitive reac- that certain chemical reactions do in avian magnetic orientation is light- tions almost always involve radicals, i.e., fact respond to applied magnetic fields. dependent—suggesting a photochemical molecules that have an odd number of The key species are radical pairs—pairs process—and is responsive to the incli- electrons and consequently an unpaired of transient radicals created simulta- nation rather than the polarity of the electron spin that may be found in one neously, such that the 2 electron spins, geomagnetic field (20–23); unlike a of 2 spin states: 1 or 2. A radical pair one on each radical, are correlated. magnetic compass needle, birds main- is a short-lived reaction intermediate They have the unique properties that tain their orientation when the ambient comprising 2 radicals formed in tandem their chemical fate is largely controlled field vector is reversed (5). whose unpaired electron spins may be ϽϽ by weak ( kBT) magnetic interactions Our aim here is to survey the radical either antiparallel (12, a singlet state, via their spin correlation and that the pair mechanism in the context of the S) or parallel (11, a triplet state, T). electron spins remain far enough from avian magnetic compass. We identify As each electron spin has an associated thermal equilibrium for long enough the key features required for efficient that the kBT objection is irrelevant. Ex- magnetoreception, comment on the like- perimental and theoretical studies of the lihood that they could occur in a biolog- Author contributions: C.T.R. and P.J.H. wrote the paper. ‘‘radical pair mechanism’’ over the last ically plausible receptor, and evaluate The authors declare no conflict of interest. 30 years have given an extraordinary the evidence for and against the radical This article is a PNAS Direct Submission. variety of information on the magnetic pair hypothesis. Throughout, the focus is 1To whom correspondence should be addressed. E-mail: properties, kinetics, and dynamics of firmly on the primary reception mecha- [email protected]. radicals and their reactions (reviewed in nism: We make no significant attempt This article contains supporting information online at www. refs. 9–13). This field of endeavor has to review the behavioral studies that led pnas.org/cgi/content/full/0711968106/DCSupplemental. come to be called ‘‘spin chemistry.’’ to and have since supported the radical © 2009 by The National Academy of Sciences of the USA www.pnas.org͞cgi͞doi͞10.1073͞pnas.0711968106 PNAS ͉ January 13, 2009 ͉ vol. 106 ͉ no. 2 ͉ 353–360 Downloaded by guest on September 24, 2021 S[A•+ B•− ] T[A•+ B•− ] steps (33). These and other possibilities f are described in the supporting informa- 3 kT tion (SI) Appendix together with com- k f 4 ∗ S ments on the nature of the reactions A B b C kS that could lead to C and subsequently 1 2 convert it back to A B. 5 A well-studied precedent for this kind A B of magnetically sensitive radical pair chemistry is provided by the initial Fig. 1. A simple reaction scheme that could form charge separation steps of bacterial pho- the basis of a compass magnetoreceptor. The spin- tosynthetic energy conversion, which correlated radical pair is depicted in red for the proceed via a series of radical ion pairs singlet state and blue for the triplet. See Key Fea- tures of a Radical Pair Magnetoreceptor: Chemis- formed by sequential electron transfers try for further details. along a chain of immobilized chlorophyll and quinone cofactors in a reaction cen- ter protein complex (15–17). Provided magnetic moment, the interconversion subsequent forward electron transfer is and chemical fates of the S and T states blocked, the recombination of the pri- can be influenced by internal and exter- mary radical pair responds to magnetic nal magnetic fields. fields in excess of Ϸ1 mT. In unblocked In chemical terms, the minimum re- reaction centers, spin correlation can be quirement for a radical pair reaction to transferred along the electron transport Fig. 2. Quantum mechanical spin dynamics sim- be sensitive to an external magnetic chain from the primary to the secondary ulations for the reaction in Fig. 1, performed as field is that at least one of the S and T radical pair (34–36), whose lifetime is described in ref. 60. (A) In the absence of the mag- states undergoes a reaction that is not also magnetically sensitive (37–39). Simi- netic field and with no recombination (green), the open to the other, usually as a conse- lar effects occur in plant photosystems. fraction of radical pairs that exist in the triplet quence of the imperative to conserve Other biological radical pair processes state, pT(t), oscillates at the frequency of the hy- perfine coupling (here 14 MHz). (B) When a weak spin angular momentum. Fig. 1 shows are much less well characterized (see SI Appendix). magnetic field is introduced (green), pT(t) shows an what is probably the simplest reaction additional, slower, modulation at the frequency of scheme possessing the essential chemical the Zeeman interaction (here 1.4 MHz). The radical Hyperfine Interactions. We now turn to features required to form the basis of a pair reactions cause pT(t) to be exponentially magnetic compass. Imagining for now the essential magnetic properties of a damped (red) and allow the reaction product (spe- that the radicals are completely immo- radical pair magnetoreceptor, focusing cies C in Fig. 1) to accumulate (blue). The applied bile, the individual reaction steps are first on detecting the presence of an ex- magnetic field (50 ␮T) results in an increased tran- as follows.
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