Environment-induced anisotropy and sensitivity of the radical pair mechanism in the avian compass

Carrillo, Alejandro; Cornelio, Marcio F.; Oliveira, M. C. de

doi:10.1103/physreve.92.012720

Cited by 18 publications

(20 citation statements)

References 37 publications

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“…There have been several theoretical treatments of spin relaxation in the context of magnetoreception, almost all of which have dealt with generic relaxation mechanisms furnished with phenomenological rate constants [36][37][38][39][40][41]. Intriguingly, a few of these studies have indicated that the compass sensitivity could be enhanced by the inclusion of certain abstract spin relaxation pathways [37,38,40,42,43]. In the following, we discuss the spin relaxation that arises from realistic spin interactions modulated by realistic protein dynamics.…”

Section: mentioning

confidence: 99%

Electron spin relaxation in cryptochrome-based magnetoreception

Kattnig

Solov’yov

Hore

2016

Phys. Chem. Chem. Phys.

173

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The magnetic compass sense of migratory birds is thought to rely on magnetically sensitive radical pairs formed photochemically in cryptochrome proteins in the retina. An important requirement of this hypothesis is that electron spin relaxation is slow enough for the Earth's magnetic field to have a significant effect on the coherent spin dynamics of the radicals. It is generally assumed that evolutionary pressure has led to protection of the electron spins from irreversible loss of coherence in order that the underlying quantum dynamics can survive in a noisy biological environment. Here, we address this question for a structurally characterized model cryptochrome expected to share many properties with the putative avian receptor protein. To this end we combine all-atom molecular dynamics simulations, Bloch-Redfield relaxation theory and spin dynamics calculations to assess the effects of spin relaxation on the performance of the protein as a compass sensor. Both flavin-tryptophan and flavin-Z˙ radical pairs are studied (Z˙ is a radical with no hyperfine interactions). Relaxation is considered to arise from modulation of hyperfine interactions by librational motions of the radicals and fluctuations in certain dihedral angles. For Arabidopsis thaliana cryptochrome 1 (AtCry1) we find that spin relaxation implies optimal radical pair lifetimes of the order of microseconds, and that flavin-Z˙ pairs are less affected by relaxation than flavin-tryptophan pairs. Our results also demonstrate that spin relaxation in isolated AtCry1 is incompatible with the long coherence times that have been postulated to explain the disruption of the avian magnetic compass sense by weak radiofrequency magnetic fields. We conclude that a cryptochrome sensor in vivo would have to differ dynamically, if not structurally, from isolated AtCry1. Our results clearly mark the limits of the current hypothesis and lead to a better understanding of the operation of radical pair magnetic sensors in noisy biological environments.

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Section: mentioning

confidence: 99%

Electron spin relaxation in cryptochrome-based magnetoreception

Kattnig

Solov’yov

Hore

2016

Phys. Chem. Chem. Phys.

173

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Section: Introductionmentioning

confidence: 99%

Electron spin relaxation can enhance the performance of a cryptochrome-based magnetic compass sensor

et al. 2016

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The radical pair model of the avian magnetoreceptor relies on long-lived electron spin coherence. Dephasing, resulting from interactions of the spins with their fluctuating environment, is generally assumed to degrade the sensitivity of this compass to the direction of the Earth's magnetic field. Here we argue that certain spin relaxation mechanisms can enhance its performance. We focus on the flavin-tryptophan radical pair in cryptochrome, currently the only candidate magnetoreceptor molecule. Correlation functions for fluctuations in the distance between the two radicals in Arabidopsis thaliana cryptochrome 1 were obtained from molecular dynamics (MD) simulations and used to calculate the spin relaxation caused by modulation of the exchange and dipolar interactions. We find that intermediate spin relaxation rates afford substantial enhancements in the sensitivity of the reaction yields to an Earth-strength magnetic field. Supported by calculations using toy radical pair models, we argue that these enhancements could be consistent with the molecular dynamics and magnetic interactions in avian cryptochromes.

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“…In support of this proposal, the photochemistry of isolated cryptochromes in vitro has been found to respond to applied magnetic fields in a manner that is quantitatively consistent with the radical pair mechanism (15). Aspects of the radical pair hypothesis have also been explored in a number of theoretical studies, the majority of which have concentrated on the magnitude of the anisotropic magnetic field effect (9,10,16,17,(19)(20)(21)(22)(23)(24)(25)(26)(27). Very little attention has been devoted to the matter we address here: the precision of the compass bearing available from a radical pair sensor (28).…”

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confidence: 99%

“…A crucial element in all such calculations is the presence of nuclear spins whose hyperfine interactions are the source of the magnetic anisotropy (8,16). Most studies have focused on idealized spin systems comprising the two electron spins, one on each radical, augmented by one or two nuclear spins (9,(21)(22)(23)(24)(25)(26)(27)34). Only a handful has attempted to deal with realistic, multinuclear radical pairs (10,16,17,20).…”

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confidence: 99%

“…Several studies have assumed, explicitly or implicitly, that the spin coherence persists for about a microsecond, i.e., the reciprocal of the electron Larmor frequency (1.4 MHz) in a 50-μT field (9,10,17,20). Either because the spin system was grossly oversimplified (9,(21)(22)(23)(24)(25)(26)(27)34), or because of this restriction on the spin coherence time, previous theoretical treatments have generally predicted the reaction yield to be a gently varying (often approximately sinusoidal) function of the orientation of the radical pair in the geomagnetic field. Although capable of delivering information on the direction of the field, such a compass would not provide a precise heading.…”

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confidence: 99%

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The quantum needle of the avian magnetic compass

Hiscock

Worster

Kattnig

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

170

223

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Migratory birds have a light-dependent magnetic compass, the mechanism of which is thought to involve radical pairs formed photochemically in cryptochrome proteins in the retina. Theoretical descriptions of this compass have thus far been unable to account for the high precision with which birds are able to detect the direction of the Earth's magnetic field. Here we use coherent spin dynamics simulations to explore the behavior of realistic models of cryptochrome-based radical pairs. We show that when the spin coherence persists for longer than a few microseconds, the output of the sensor contains a sharp feature, referred to as a spike. The spike arises from avoided crossings of the quantum mechanical spin energy-levels of radicals formed in cryptochromes. Such a feature could deliver a heading precision sufficient to explain the navigational behavior of migratory birds in the wild. Our results (i) afford new insights into radical pair magnetoreception, (ii) suggest ways in which the performance of the compass could have been optimized by evolution, (iii) may provide the beginnings of an explanation for the magnetic disorientation of migratory birds exposed to anthropogenic electromagnetic noise, and (iv) suggest that radical pair magnetoreception may be more of a quantum biology phenomenon than previously realized. magnetic compass | magnetoreception | migratory birds | quantum biology | radical pair mechanism M igratory birds have a light-dependent magnetic compass (1-4). The primary sensory receptors are located in the eyes (2, 3, 5-7), and directional information is processed bilaterally in a small part of the forebrain accessed via the thalamofugal visual pathway. The evidence currently points to a chemical sensing mechanism based on photo-induced radical pairs in cryptochrome flavoproteins in the retina (8-18). Anisotropic magnetic interactions within the radicals are thought to give rise to intracellular levels of a cryptochrome signaling state that depend on the orientation of the bird's head in the Earth's magnetic field (8,9,19). In support of this proposal, the photochemistry of isolated cryptochromes in vitro has been found to respond to applied magnetic fields in a manner that is quantitatively consistent with the radical pair mechanism (15). Aspects of the radical pair hypothesis have also been explored in a number of theoretical studies, the majority of which have concentrated on the magnitude of the anisotropic magnetic field effect (9,10,16,17,(19)(20)(21)(22)(23)(24)(25)(26)(27). Very little attention has been devoted to the matter we address here: the precision of the compass bearing available from a radical pair sensor (28).To migrate successfully over large distances, it is not sufficient simply to distinguish north from south (or poleward from equatorward) (29). A bar-tailed godwit (Limosa lapponica baueri), for example, was tracked by satellite flying from Alaska to New Zealand in a single 11,000-km nonstop flight across the Pacific Ocean (30). A directional error of more than a few degre...

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Environment-induced anisotropy and sensitivity of the radical pair mechanism in the avian compass

Cited by 18 publications

References 37 publications

Electron spin relaxation in cryptochrome-based magnetoreception

Electron spin relaxation in cryptochrome-based magnetoreception

Electron spin relaxation can enhance the performance of a cryptochrome-based magnetic compass sensor

The quantum needle of the avian magnetic compass

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