Solvent Driving Force Ensures Fast Formation of a Persistent and Well-Separated Radical Pair in Plant Cryptochrome

Lüdemann, Gesa; Solov’yov, Ilia A.; Kubař, Tomáš; Elstner, Marcus

doi:10.1021/ja510550g

Cited by 81 publications

(209 citation statements)

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“…This radical pair is short-lived, as a second and then third tryptophan residue transfer electrons sequentially, leading to a radical pair formation between FAD •− and 42434445. This activation mechanism of cryptochrome is depicted in Fig.…”

Section: Resultsmentioning

confidence: 95%

Multiscale description of avian migration: from chemical compass to behaviour modeling

Pedersen

Nielsen

Solov’yov

2016

Sci Rep

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Despite decades of research the puzzle of the magnetic sense of migratory songbirds has still not been unveiled. Although the problem really needs a multiscale description, most of the individual research efforts were focused on single scale investigations. Here we seek to establish a multiscale link between some of the scales involved, and in particular construct a bridge between electron spin dynamics and migratory bird behaviour. In order to do that, we first consider a model cyclic reaction scheme that could form the basis of the avian magnetic compass. This reaction features a fast spin-dependent process which leads to an unusually precise compass. We then propose how the reaction could be realized in a realistic molecular environment, and argue that it is consistent with the known facts about avian magnetoreception. Finally we show how the microscopic dynamics of spins could possibly be interpreted by a migrating bird and used for the navigational purpose.

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Section: Resultsmentioning

confidence: 95%

Multiscale description of avian migration: from chemical compass to behaviour modeling

Pedersen

Nielsen

Solov’yov

2016

Sci Rep

Self Cite

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“…The primary sensory receptors are located in the eyes (2,3,(5)(6)(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)(9)(10)(11)(12)(13)(14)(15)(16)(17)(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).…”

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confidence: 99%

The quantum needle of the avian magnetic compass

Hiscock

Worster

Kattnig

et al. 2016

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

171

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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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“…• [11], which have been successfully employed in several MD studies of cryptochrome [11,34,35]. A time step of 2 fs was used and the temperature was kept at 300 K using the Langevin thermostat.…”

Section: Simulation Protocolmentioning

confidence: 99%

“…1 and conventionally labelled, in order of increasing distance from the FAD, as WA, WB, WC and WD. Radical pairs involving FAD and either WA or WB have lifetimes of less than a nanosecond, which precludes sensitivity to the geomagnetic field [11]. [FAD • WC…”

Section: Introductionmentioning

confidence: 99%

Ascorbic acid may not be involved in cryptochrome-based magnetoreception

Nielsen

Kattnig

Sjulstok

et al. 2017

J. R. Soc. Interface.

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Seventeen years after it was originally suggested, the photoreceptor protein cryptochrome remains the most probable host for the radical pair intermediates that are thought to be the sensors in the avian magnetic compass. Although evidence in favour of this hypothesis is accumulating, the intracellular interaction partners of the sensory protein are still unknown. It has been suggested that ascorbate ions could interact with surface-exposed tryptophan radicals in photoactivated cryptochromes, and so lead to the formation of a radical pair comprised of the reduced form of the flavin adenine dinucleotide cofactor, FAD• , and the ascorbate radical, Asc shown that ascorbate ions are expected to bind near the tryptophan radicals for periods of a few nanoseconds. The rate at which these encounters happen is low, and it is therefore concluded that ascorbate ions are unlikely to be involved in magnetoreception if the ascorbate concentration is only on the order of 100 M or less.3

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Solvent Driving Force Ensures Fast Formation of a Persistent and Well-Separated Radical Pair in Plant Cryptochrome

Cited by 81 publications

References 88 publications

Multiscale description of avian migration: from chemical compass to behaviour modeling

Multiscale description of avian migration: from chemical compass to behaviour modeling

The quantum needle of the avian magnetic compass

Ascorbic acid may not be involved in cryptochrome-based magnetoreception

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