A large variety of animals has the ability to sense the geomagnetic field and utilize it as a source of directional (compass) information. It is not known by which biophysical mechanism this magnetoreception is achieved. We investigate the possibility that magnetoreception involves radical-pair processes that are governed by anisotropic hyperfine coupling between (unpaired) electron and nuclear spins. We will show theoretically that fields of geomagnetic field strength and weaker can produce significantly different reaction yields for different alignments of the radical pairs with the magnetic field. As a model for a magnetic sensory organ we propose a system of radical pairs being 1) orientationally ordered in a molecular substrate and 2) exhibiting changes in the reaction yields that affect the visual transduction pathway. We evaluate three-dimensional visual modulation patterns that can arise from the influence of the geomagnetic field on radical-pair systems. The variations of these patterns with orientation and field strength can furnish the magnetic compass ability of birds with the same characteristics as observed in behavioral experiments. We propose that the recently discovered photoreceptor cryptochrome is part of the magnetoreception system and suggest further studies to prove or disprove this hypothesis.

Cryptochromes are flavoprotein photoreceptors first identified in Arabidopsis thaliana, where they play key roles in growth and development. Subsequently identified in prokaryotes, archaea, and many eukaryotes, cryptochromes function in the animal circadian clock and are proposed as magnetoreceptors in migratory birds. Cryptochromes are closely structurally related to photolyases, evolutionarily ancient flavoproteins that catalyze light-dependent DNA repair. Here, we review the structural, photochemical, and molecular properties of cry-DASH, plant, and animal cryptochromes in relation to biological signaling mechanisms and uncover common features that may contribute to better understanding the function of cryptochromes in diverse systems including in man.

Migratory birds are known to use the geomagnetic field as a source of compass information. There are two competing hypotheses for the primary process underlying the avian magnetic compass, one involving magnetite, the other a magnetically sensitive chemical reaction. Here we show that oscillating magnetic fields disrupt the magnetic orientation behaviour of migratory birds. Robins were disoriented when exposed to a vertically aligned broadband (0.1-10 MHz) or a single-frequency (7-MHz) field in addition to the geomagnetic field. Moreover, in the 7-MHz oscillating field, this effect depended on the angle between the oscillating and the geomagnetic fields. The birds exhibited seasonally appropriate migratory orientation when the oscillating field was parallel to the geomagnetic field, but were disoriented when it was presented at a 24 degrees or 48 degrees angle. These results are consistent with a resonance effect on singlet-triplet transitions and suggest a magnetic compass based on a radical-pair mechanism.

Absorption of light by light-harvesting complexes and transfer of electronic excitation to the photosynthetic reaction center (RC) constitute the primary light-harvesting process of photosynthesis. This process is investigated on the basis of an atomic level structure of the so-called photosynthetic unit of the photosynthetic bacterium Rhodobacter sphaeroides. The photosynthetic unit combines in the intracytoplasmic membrane a nanometric assembly of three pigment-protein complexes: (i) the photosynthetic reaction center, (ii) a ringshaped light-harvesting complex LH-I, and (iii) multiple copies of a similar complex, LH-II. The unit has been modeled using the known structure of (i) and for (ii) a model structure complexed appropriately with (i); for (iii) the structure of LH-II of Rhodospirillum molischianum is substituted. The model describes in detail the organization of chromophores involved in primary light absorption and excitation transfer: a hierarchy of ring-shaped bacteriochlorophyll aggregates that surround four centrally located bacteriochlorophylls of the photosynthetic reaction center. The bacteriochlorophylls involved in the overall transfer are found in a coplanar arrangement. On the basis of the modeled structure a quantum-mechanical description of the entire lightharvesting process is developed. For this purpose an effective Hamiltonian is established a priori and then employed to describe the LH-II f LH-II f LH-I f RC cascade of excitation transfer. The transfer times calculated are in agreement with measured transfer times. The results suggest that excitons are the key carriers of the excitation transferred; i.e., electronic excitations are coherently delocalized in the photosynthetic unit. This suggestion is corroborated by an investigation of the effect of inhomogeneous broadening on the predicted excitons in LH-II and LH-I, an effect that is found to be significant but small. A particularly important role is played by the lowest energy excitons to which the circular arrangement of bacteriochlorophylls imparts vanishing oscillator strength. Despite the lack of oscillator strength, the low-energy excitons are well suited for exciton transfer on a subpicosecond and picosecond time scale. The accessory bacteriochlorophylls of the photosynthetic reaction center are found to be critical for the LH-I f RC transfer, which would take several hundred picoseconds without these bacteriochlorophylls.

The avian magnetic compass has been well characterized in behavioral tests: it is an "inclination compass" based on the inclination of the field lines rather than on the polarity, and its operation requires short-wavelength light. The "radical pair" model suggests that these properties reflect the use of specialized photopigments in the primary process of magnetoreception; it has recently been supported by experimental evidence indicating a role of magnetically sensitive radical-pair processes in the avian magnetic compass. In a multidisciplinary approach subjecting migratory birds to oscillating fields and using their orientation responses as a criterion for unhindered magnetoreception, we identify key features of the underlying receptor molecules. Our observation of resonance effects at specific frequencies, combined with new theoretical considerations and calculations, indicate that birds use a radical pair with special properties that is optimally designed as a receptor in a biological compass. This radical pair design might be realized by cryptochrome photoreceptors if paired with molecular oxygen as a reaction partner.