Radical-Pair-Based Magnetoreception Amplified by Radical Scavenging: Resilience to Spin Relaxation.

Daniel R Kattnig

doi:10.1021/acs.jpcb.7b07672

Abstract

Birds and several other species are equipped with the remarkable ability to sense the geomagnetic field for the purpose of navigation and orientation. The primary detection mechanism of this compass sense is uncertain but appears to originate from a truly quantum process involving spin-correlated radical pairs. In order to elicit sensitivity to weak magnetic fields, such as the Earth's magnetic field, the underlying spin dynamics must be protected from fast decoherence. In this work, we elucidate the effects of spin relaxation on a recently suggested reaction scheme involving three radicals, instead of a radical pair, doublet-quartet interconversion under magnetic interactions, and a spin-selective scavenging reaction. We show that, besides giving rise to a vastly enhanced reaction anisotropy, this extended reaction scheme is more resilient to spin relaxation than the conventional radical pair mechanism. Surprisingly, the anisotropic magnetic field effect can be enhanced by fast spin relaxation in one of the radicals of the primary pair. We discuss this finding in the context of magnetoreception. Radical scavenging can protect the spin system against fast spin relaxation in one of the radicals, thereby providing a credible model to the involvement of fast relaxing radical pairs, such as FADH•/O2•-, in radical-pair based magnetoreception. This finding will help explain behavioral observations that seem incompatible with the previously proposed flavin semiquinone/tryptophanyl radical pair.

Highlights

A variety of animals, most notably many birds, appear to employ a truly quantum mechanism to detect the geomagnetic field
Magnetosensitivity can result from a process that, according to the classical radical pair mechanism (RPM), entails three essential steps, which are summarized in Figure 1a:11-13 First, a RP is generated, typically in a pure spin state, e.g. 1[A– – B+]
The forward rate constant kf was fixed at 0.1 μs 1, yielding a RP lifetime of 10 s in the absence of spin-selective charge recombination or scavenging. This is motivated by a recent study of spin relaxation in AtCry, suggesting that the magnetic field effects (MFEs) would be strongly attenuated for longer-lived RPs.[27]

Summary

Introduction

A variety of animals, most notably many (migratory) birds, appear to employ a truly quantum mechanism to detect the geomagnetic field. Magnetosensitivity can result from a process that, according to the classical radical pair mechanism (RPM), entails three essential steps, which are summarized in Figure 1a:11-13 First, a RP is generated, typically in a pure spin state, e.g. 1[A– – B+] In vitro, this step is realized by photoinduced electron transfer along three or four highly conserved tryptophan residues, the so-called tryptophan triad or tetrad, to the noncovalently bound, oxidized FAD cofactor.[14,15,16] In vivo, the formation of the RP could result from the dark reoxidation of the fully reduced FAD, FADH−, accumulated via an upstream light-dependent reduction route (e.g. see Figure 1 of ref 17 and Figure 5 of this work).[17,18,19,20,21,22,23] Second, the RP undergoes coherent singlettriplet interconversion at a rate dictated by anisotropic hyperfine interactions with surrounding magnetic nuclei, the Zeeman interaction with the Earth’s magnetic field, and the exchange and electron-electron dipolar coupling. Spin-selective reactions of the RP render the yield of a signalling state, which derives from the spin-correlated RP, dependent on the above-mentioned singlet-triplet interconversion process

Results

Discussion

Conclusion