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Quantum Compass of Migratory Birds

 

 

 

the radical pair is initially in an electronic singlet state, [FAD^•− TrpCH^•+] (Henbest et al., 2008; Weber

et al., 2010; Maeda et al., 2012). Tis form of the protein is a coherent superposition of the eigenstates

of the spin Hamiltonian which comprises the Zeeman, hyperfne, exchange, and dipolar interactions

of the electron spins. As a consequence, the radical pairs oscillate coherently between the singlet and

triplet states, a process that manifests itself in the yields of subsequent spin-selective reactions of the

radicals. In particular, when the protein is immobilized, the anisotropy of the electron-nuclear hyper­

fne coupling (HFC) interactions causes the reaction product yields to depend on the orientation of the

protein with respect to an external magnetic feld.

Sheppard et al. (2017) reported spectroscopic measurements of photo-induced FAD and Trp radi­

cals in recombinantly expressed, purifed DmCRY. In brief, a combination of transient absorption and

broadband cavity-enhanced absorption spectroscopy has been employed to explore the efects of exter­

nal magnetic felds (of up to 22 mT) on the key species involved in the photocycle of DmCRY (Sheppard

et al., 2017). Details of these techniques can be found elsewhere (Maeda et al.. 2012; Neil et al., 2014).

Te protein concentration (∼50 μM), temperature (267–278 K) and glycerol content (∼50% for transient

absorption measurements and 20% for the cavity-enhanced absorbance experiments) of the solutions

were chosen to optimize the magnetic responses.

In the case of the AtCRY1, the distance of the fnally generated radical pair [FADH^• TyrO^•] is 16 Å

or more, and the lifetime of the radical pair is extended by suppressing charge recombination (Giovani

et al., 2003). In the case of the migratory bird CRY, its structure and function might be similar or almost

the same as those of the AtCRY, and it is estimated that Try could contribute to the stability of radical

state FADH^• (Liedvogel et al., 2007). Te lifetime of the fnal radical pair [FADH^• TyrO^•] is reported to

be 14 ms at room temperature (Liedvogel et al., 2007).

In the case of the migratory bird CRY (gwCRY1a), it is uncertain because the exact structure has

not been clarifed, but when estimated from the amino acid sequences of the CRY, there is a possi­

bility that aspartic acid (Asp) is located in the vicinity of FAD, and the favin radical state FADH^• is

stabilized (Liedvogel et al., 2007). It is speculated that it may have acquired the function of a magnetic

compass (Liedvogel et al., 2007). Furthermore, in the migratory bird gwCRY1a (Liedvogel et al., 2007)

and AtCRY1 (Giovani et al., 2003), where FADH^• is a key radical, electron transfer from Try to a trypto­

phanyl radical, Trp^• (generated by electron transfer from Trp to FAD) has been reported. Here, a favin

radical, FADH^• has broad absorption from 500 to 650 nm, 5 ms half-life in AtCRY1, 14 ms lifetime in

gwCRY1a, and Trp^• has a narrow component from 500 to 550 nm, 1 ms half-life in AtCRY1, 4 ms lifetime

in gwCRY1a (Liedvogel et al., 2007). Focusing on the function of CRY, the form of FAD in the magnetic

compass for avian bird CRY is estimated to be FADH^• (Liedvogel et al., 2007).

4.4.2 Magnetic Sense and Cryptochrome

It is said that a blue light-sensing protein called “cryptochrome (CRY)” in the retina of the eye plays

an important role as a magnetic sensor or magnetoreceptor (Ritz et al., 2000, 2004, 2009; Möller et al.,

2004; Mouritsen et al., 2004; Mouritsen and Ritz, 2005; Zapka et al., 2009; Mouritsen and Hore, 2012;

Lau et al., 2012; Wiltschko and Wiltschko, 2014, 2021; Bolte et al., 2016; Kerpal et al., 2019; Wiltschko

et al., 2021). CRY proteins are also components of the central circadian clockwork (Yuan et al., 2007)

and are closely related to the light-dependent DNA repair enzymes, the photolyases (Cashmore, 2003).

It is reported that the CRY is fngered as the smoking gun in the exquisite magnetic reception of birds

(Roberts, 2016). As a putative magnetoreceptor, fve diferent isoform CRYs (CRY1a, CRY1b, CRY2,

CRY4a, and CRY4b) have been identifed in the retinae of several bird species. CRY1a (Liedvogel

et al., 2007; Nießner et al., 2011) is found from garden warblers (Sylvia borin) and European robins.

CRY1b (Bolte et al., 2016; Nießner et al., 2016) is from European robins, migratory northern wheatears

(Oenanthe oenanthe), and homing pigeons. CRY2 (Mouritsen et al., 2004) is from migratory garden

warblers. CRY4 (Günther et al., 2018; Pinzon-Rodriguez et al., 2018; Hochstoeger et al., 2020; Wu et al.,

2020) is from European robins.