Kiminori Maeda

Chemical compass model of avian magnetoreception

Approximately 50 species, including birds, mammals, reptiles, amphibians, fish, crustaceans and insects, are known to use the Earth’s magnetic field for orientation and navigation. Birds in particular have been intensively studied, but the biophysical mechanisms that underlie the avian magnetic compass are still poorly understood. One proposal, based on magnetically sensitive free radical reactions, is gaining support despite the fact that no chemical reaction in vitro has been shown to respond to magnetic fields as weak as the Earth’s (∼50 μT) or to be sensitive to the direction of such a field. Here we use spectroscopic observation of a carotenoid–porphyrin–fullerene model system to demonstrate that the lifetime of a photochemically formed radical pair is changed by application of ≤50 μT magnetic fields, and to measure the anisotropic chemical response that is essential for its operation as a chemical compass sensor. These experiments establish the feasibility of chemical magnetoreception and give insight into the structural and dynamic design features required for optimal detection of the direction of the Earth’s magnetic field.

Magnetically sensitive light-induced reactions in cryptochrome are consistent with its proposed role as a magnetoreceptor

Among the biological phenomena that fall within the emerging field of “quantum biology” is the suggestion that magnetically sensitive chemical reactions are responsible for the magnetic compass of migratory birds. It has been proposed that transient radical pairs are formed by photo-induced electron transfer reactions in cryptochrome proteins and that their coherent spin dynamics are influenced by the geomagnetic field leading to changes in the quantum yield of the signaling state of the protein. Despite a variety of supporting evidence, it is still not clear whether cryptochromes have the properties required to respond to magnetic interactions orders of magnitude weaker than the thermal energy, kBT. Here we demonstrate that the kinetics and quantum yields of photo-induced flavin—tryptophan radical pairs in cryptochrome are indeed magnetically sensitive. The mechanistic origin of the magnetic field effect is clarified, its dependence on the strength of the magnetic field measured, and the rates of relevant spin-dependent, spin-independent, and spin-decoherence processes determined. We argue that cryptochrome is fit for purpose as a chemical magnetoreceptor.

Chemical Magnetoreception: Bird Cryptochrome 1a Is Excited by Blue Light and Forms Long-Lived Radical-Pairs

Cryptochromes (Cry) have been suggested to form the basis of light-dependent magnetic compass orientation in birds. However, to function as magnetic compass sensors, the cryptochromes of migratory birds must possess a number of key biophysical characteristics. Most importantly, absorption of blue light must produce radical pairs with lifetimes longer than about a microsecond. Cryptochrome 1a (gwCry1a) and the photolyase-homology-region of Cry1 (gwCry1-PHR) from the migratory garden warbler were recombinantly expressed and purified from a baculovirus/Sf9 cell expression system. Transient absorption measurements show that these flavoproteins are indeed excited by light in the blue spectral range leading to the formation of radicals with millisecond lifetimes. These biophysical characteristics suggest that gwCry1a is ideally suited as a primary light-mediated, radical-pair-based magnetic compass receptor.

Magnetic-field effect on the photoactivation reaction of Escherichia coli DNA photolyase

One of the two principal hypotheses put forward to explain the primary magnetoreception event underlying the magnetic compass sense of migratory birds is based on a magnetically sensitive chemical reaction. It has been proposed that a spin-correlated radical pair is produced photochemically in a cryptochrome and that the rates and yields of the subsequent chemical reactions depend on the orientation of the protein in the Earths magnetic field. The suitability of cryptochrome for this purpose has been argued, in part, by analogy with DNA photolyase, although no effects of applied magnetic fields have yet been reported for any member of the cryptochrome/photolyase family. Here, we demonstrate a magnetic-field effect on the photochemical yield of a flavin–tryptophan radical pair in Escherichia coli photolyase. This result provides a proof of principle that photolyases, and most likely by extension also cryptochromes, have the fundamental properties needed to form the basis of a magnetic compass.

Effect of magnetic fields on cryptochrome-dependent responses in Arabidopsis thaliana

The scientific literature describing the effects of weak magnetic fields on living systems contains a plethora of contradictory reports, few successful independent replication studies and a dearth of plausible biophysical interaction mechanisms. Most such investigations have been unsystematic, devoid of testable theoretical predictions and, ultimately, unconvincing. A recent study, of magnetic responses in the model plant Arabidopsis thaliana, however, stands out; it has a clear hypothesis—that seedling growth is magnetically sensitive as a result of photoinduced radical-pair reactions in cryptochrome photoreceptors—tested by measuring several cryptochrome-dependent responses, all of which proved to be enhanced in a magnetic field of intensity 500 μT. The potential importance of this study in the debate on putative effects of extremely low-frequency electromagnetic fields on human health prompted us to subject it to the ‘gold standard’ of independent replication. With experimental conditions chosen to match those of the original study, we have measured hypocotyl lengths and anthocyanin accumulation for Arabidopsis seedlings grown in a 500 μT magnetic field, with simultaneous control experiments at 50 μT. Additionally, we have determined hypocotyl lengths of plants grown in 50 μT, 1 mT and approximately 100 mT magnetic fields (with zero-field controls), measured gene (CHS, HY5 and GST) expression levels, investigated blue-light intensity effects and explored the influence of sucrose in the growth medium. In no case were consistent, statistically significant magnetic field responses detected.

Spin-correlated radical pairs in micellar systems: mechanism of CIDEP and the micelle size dependence

Abstract A new model of time-resolved EPR in micellized radical pairs is introduced. The model is based on numerical integration of the master Liouville equation for spin-correlated (micellized) pairs and free (escaped) radicals. The diffusion of radicals is considered in terms of a supercage model. This approach is used to analyze data on laser flash photolysis of 13 C-carbonyl labelled ketone α-deoxybenzoin in aqueous sodium alkyl (10–12) sulphate solutions. EPR lines of 13 C-benzoyl radicals exhibit antiphase structure (APS) typical of spin-correlated pairs. Due to very large APS splitting, 0.8–1.5 mT, the ST 0 polarized lines from free benzoyl radicals can be isolated spectrally. The observed line shape of the APS cannot be accounted for in the standard model of effective exchange potential. The shape of the APS is shown to be controlled by spin exchange relaxation in micellized pairs.

Improved photo-CIDNP methods for studying protein structure and folding.

Two new techniques offering considerable improvements in the quality of 1H photo-CIDNP spectra of proteins are demonstrated. Both focus on the problem of progressive photo-degradation of the flavin dye used to generate polarization in exposed tryptophan, tyrosine and histidine side-chains. One approach uses rapid addition and removal of protein/flavin solution between light flashes to mix the NMR sample and introduce fresh dye into the laser-irradiated region. The other involves chemical oxidation of photo-reduced flavin by the addition of hydrogen peroxide. In both cases a larger number of scans can be accumulated before the flavin is exhausted than would otherwise be possible. The techniques are demonstrated by 600 MHz CIDNP-NOESY spectroscopy of bovine holo-α-lactalbumin, and by real-time CIDNP observation of the refolding of bovine apo-α-lactalbumin following rapid dilution from a high concentration of chemical denaturant.

Consistent Treatment of Spin-Selective Recombination of a Radical Pair Confirms the Haberkorn Approach

In the present work, we have shown that consistent derivation of the kinetic equations describing the electron spin-selective recombination of radical pairs confirms the conventional Haberkorn approach. The derivation has been based on considering the interaction of the reactive system (radical pair and product state) with the thermal bath. The consistency of this approach has also been substantiated by numerical simulations performed for the purely quantum mechanical model of the recombining radical pair. Finally, we have shown that the quantum Zeno effect on radical pair recombination is not an exclusive feature of the approach recently proposed by Kominis, as it should be present at any rate of the singlet-triplet dephasing in the radical pair, which always accompanies the recombination process.

Spin-selective recombination kinetics of a model chemical magnetoreceptor

We determine the spin-selective kinetics of a carotenoid-porphyrin-fullerene triad that has previously been used to establish the principle that a photochemical reaction could form the basis of the magnetic compass sensor of migratory birds and show that its magnetic sensitivity can be understood without invoking quantum Zeno effects.

The time-resolved absorption-detected magnetic resonance spectrum of the polymethylene linked biradical: effect of the exchange integral

Abstract The time-resolved absorption-detected magnetic resonance spectrum of the polymethylene linked biradical generated in the photolysis of α -(xanthene-2-carbonyloxy)- ω -(xanthene-2-carbonyloxy)dodecane was observed. The central part of the spectrum shows an increase in the absorbance by applying high microwave power. This is rationalized by the deceleration of the intersystem crossing due to the state locking that serves to slow down the intramolecular recombination reaction. Both wing portions show an increase in the recombination rate by microwave radiation, i.e. acceleration of the intersystem crossing. This is ascribed to transitions from the |T +1 > and |T −1 > states to a singlet state having a slight |T 0 > character. We propose that the broadness of the time resolved spectrum is due to the wide distribution of the exchange integral and its fluctuation (modulated exchange integral) by the motion of the polymethylene chain.