Light-dependent magnetoreception in birds: the crucial step occurs in the dark

The Radical Pair Model proposes that the avian magnetic compass is based on spin-chemical processes: since the ratio between the two spin states singlet and triplet of radical pairs depends on their alignment in the magnetic field, it can provide information on magnetic directions. Cryptochromes, blue light-absorbing flavoproteins, with flavin adenine dinucleotide as chromophore, are suggested as molecules forming the radical pairs underlying magnetoreception. When activated by light, cryptochromes undergo a redox cycle, in the course of which radical pairs are generated during photo-reduction as well as during light-independent re-oxidation. This raised the question as to which radical pair is crucial for mediating magnetic directions. Here, we present the results from behavioural experiments with intermittent light and magnetic field pulses that clearly show that magnetoreception is possible in the dark interval, pointing to the radical pair formed during flavin re-oxidation. This differs from the mechanism considered for cryptochrome signalling the presence of light and rules out most current models of an avian magnetic compass based on the radical pair generated during photo-reduction. Using the radical pair formed during re-oxidation may represent a specific adaptation of the avian magnetic compass.

[1]  S. Iwai,et al.  Discovery and functional analysis of a 4th electron-transferring tryptophan conserved exclusively in animal cryptochromes and (6-4) photolyases. , 2015, Chemical communications.

[2]  H. Burda,et al.  Magnetically induced behaviour of ferritin corpuscles in avian ears: can cuticulosomes function as magnetosomes? , 2015, Journal of The Royal Society Interface.

[3]  L. Peichl,et al.  Magnetoreception in birds: I. Immunohistochemical studies concerning the cryptochrome cycle , 2014, Journal of Experimental Biology.

[4]  W. Wiltschko,et al.  Magnetoreception in birds: II. Behavioural experiments concerning the cryptochrome cycle , 2014, Journal of Experimental Biology.

[5]  K. Kavokin,et al.  Magnetic orientation of garden warblers (Sylvia borin) under 1.4 MHz radiofrequency magnetic field , 2014, Journal of The Royal Society Interface.

[6]  W. Wiltschko,et al.  Sensing Magnetic Directions in Birds: Radical Pair Processes Involving Cryptochrome , 2014, Biosensors.

[7]  P. Hore,et al.  Alternative radical pairs for cryptochrome-based magnetoreception , 2014, Journal of The Royal Society Interface.

[8]  H. Mouritsen,et al.  Anthropogenic electromagnetic noise disrupts magnetic compass orientation in a migratory bird , 2014, Nature.

[9]  L. Peichl,et al.  Magnetoreception: activated cryptochrome 1a concurs with magnetic orientation in birds , 2013, Journal of The Royal Society Interface.

[10]  H. Mouritsen,et al.  Migratory Reed Warblers Need Intact Trigeminal Nerves to Correct for a 1,000 km Eastward Displacement , 2013, PloS one.

[11]  D. Keays,et al.  An Iron-Rich Organelle in the Cuticular Plate of Avian Hair Cells , 2013, Current Biology.

[12]  R. Bittl,et al.  Lifetimes of Arabidopsis cryptochrome signaling states in vivo. , 2013, The Plant journal : for cell and molecular biology.

[13]  W. Wiltschko,et al.  Interactions between the visual and the magnetoreception system: Different effects of bichromatic light regimes on the directional behavior of migratory birds , 2013, Journal of Physiology-Paris.

[14]  W. Wiltschko,et al.  The magnetite-based receptors in the beak of birds and their role in avian navigation , 2012, Journal of Comparative Physiology A.

[15]  K. Schulten,et al.  Decrypting cryptochrome: revealing the molecular identity of the photoactivation reaction. , 2012, Journal of the American Chemical Society.

[16]  Jeremy Shaw,et al.  Clusters of iron-rich cells in the upper beak of pigeons are macrophages not magnetosensitive neurons , 2012, Nature.

[17]  Stefan Weber,et al.  Magnetically sensitive light-induced reactions in cryptochrome are consistent with its proposed role as a magnetoreceptor , 2012, Proceedings of the National Academy of Sciences.

[18]  K. Schulten,et al.  Reaction kinetics and mechanism of magnetic field effects in cryptochrome. , 2011, The journal of physical chemistry. B.

[19]  L. Peichl,et al.  Avian Ultraviolet/Violet Cones Identified as Probable Magnetoreceptors , 2011, PloS one.

[20]  T. Ritz,et al.  The cryptochromes: blue light photoreceptors in plants and animals. , 2011, Annual review of plant biology.

[21]  Margaret Ahmad,et al.  Light-activated Cryptochrome Reacts with Molecular Oxygen to Form a Flavin–Superoxide Radical Pair Consistent with Magnetoreception* , 2011, The Journal of Biological Chemistry.

[22]  Le-Qing Wu,et al.  Magnetoreception in an Avian Brain in Part Mediated by Inner Ear Lagena , 2011, Current Biology.

[23]  E. Getzoff,et al.  Origin of light-induced spin-correlated radical pairs in cryptochrome. , 2010, The journal of physical chemistry. B.

[24]  W. Wiltschko,et al.  The Role of the Magnetite-Based Receptors in the Beak in Pigeon Homing , 2010, Current Biology.

[25]  J. Wild,et al.  Magnetic field changes activate the trigeminal brainstem complex in a migratory bird , 2010, Proceedings of the National Academy of Sciences.

[26]  T. Ritz,et al.  Photoreceptor-based magnetoreception: optimal design of receptor molecules, cells, and neuronal processing , 2010, Journal of The Royal Society Interface.

[27]  W. Wiltschko,et al.  Directional orientation of birds by the magnetic field under different light conditions , 2010, Journal of The Royal Society Interface.

[28]  Henrik Mouritsen,et al.  Avian Magnetoreception: Elaborate Iron Mineral Containing Dendrites in the Upper Beak Seem to Be a Common Feature of Birds , 2010, PloS one.

[29]  Joseph L. Kirschvink,et al.  Biophysics of magnetic orientation: strengthening the interface between theory and experimental design , 2010, Journal of The Royal Society Interface.

[30]  Henrik Mouritsen,et al.  Visual but not trigeminal mediation of magnetic compass information in a migratory bird , 2009, Nature.

[31]  W. Wiltschko,et al.  Oscillating magnetic field disrupts magnetic orientation in Zebra finches, Taeniopygia guttata , 2009, Frontiers in Zoology.

[32]  M. Frisch,et al.  Relativistic interactions in the radical pair model of magnetic field sense in CRY-1 protein of Arabidopsis thaliana. , 2009, The journal of physical chemistry. A.

[33]  C. Timmel,et al.  Possible involvement of superoxide and dioxygen with cryptochrome in avian magnetoreception: Origin of Zeeman resonances observed by in vivo EPR spectroscopy , 2009 .

[34]  Wolfgang Wiltschko,et al.  Avian orientation: the pulse effect is mediated by the magnetite receptors in the upper beak , 2009, Proceedings of the Royal Society B: Biological Sciences.

[35]  Klaus Schulten,et al.  Magnetoreception through cryptochrome may involve superoxide. , 2009, Biophysical journal.

[36]  Thorsten Ritz,et al.  Magnetic compass of birds is based on a molecule with optimal directional sensitivity. , 2009, Biophysical journal.

[37]  K. Kavokin The puzzle of magnetic resonance effect on the magnetic compass of migratory birds , 2008, Bioelectromagnetics.

[38]  Ilya Kuprov,et al.  Chemical compass model of avian magnetoreception , 2008, Nature.

[39]  Wolfgang Wiltschko,et al.  Orientation of Birds in Total Darkness , 2008, Current Biology.

[40]  T. Ritz,et al.  The magnetic compass of domestic chickens, Gallus gallus , 2007, Journal of Experimental Biology.

[41]  R. Bittl,et al.  The Signaling State of Arabidopsis Cryptochrome 2 Contains Flavin Semiquinone* , 2007, Journal of Biological Chemistry.

[42]  Christiane R Timmel,et al.  Determination of radical re-encounter probability distributions from magnetic field effects on reaction yields. , 2007, Journal of the American Chemical Society.

[43]  E. Wolf,et al.  A Novel Photoreaction Mechanism for the Circadian Blue Light Photoreceptor Drosophila Cryptochrome* , 2007, Journal of Biological Chemistry.

[44]  Wei Lin,et al.  Testing for the presence of magnetite in the upper-beak skin of homing pigeons , 2007, BioMetals.

[45]  Filip Vandenbussche,et al.  Cryptochrome Blue Light Photoreceptors Are Activated through Interconversion of Flavin Redox States* , 2007, Journal of Biological Chemistry.

[46]  P. Kukura,et al.  Radio frequency magnetic field effects on a radical recombination reaction: a diagnostic test for the radical pair mechanism. , 2004, Journal of the American Chemical Society.

[47]  Thorsten Ritz,et al.  Resonance effects indicate a radical-pair mechanism for avian magnetic compass , 2004, Nature.

[48]  W. Wiltschko,et al.  Ultrastructural analysis of a putative magnetoreceptor in the beak of homing pigeons , 2003, The Journal of comparative neurology.

[49]  J. Wild,et al.  Trigeminally innervated iron-containing structures in the beak of homing pigeons, and other birds , 2001, Brain Research.

[50]  K. Schulten,et al.  A model for photoreceptor-based magnetoreception in birds. , 2000, Biophysical journal.

[51]  W. Wiltschko,et al.  The effect of yellow and blue light on magnetic compass orientation in European robins, Erithacus rubecula , 1999, Journal of Comparative Physiology A.

[52]  W. Wiltschko,et al.  Migratory orientation of European Robins is affected by the wavelength of light as well as by a magnetic pulse , 1995, Journal of Comparative Physiology A.

[53]  Wolfgang Wiltschko,et al.  Red light disrupts magnetic orientation of migratory birds , 1993, Nature.

[54]  R. Beason,et al.  Responses to small magnetic variations by the trigeminal system of the bobolink , 1990, Brain Research Bulletin.

[55]  W. Wiltschko,et al.  Disorientation of inexperienced young pigeons after transportation in total darkness , 1981, Nature.

[56]  W. Wiltschko,et al.  Magnetic Compass of European Robins , 1972, Science.

[57]  Stephen T. Emlen,et al.  A TECHNIQUE FOR RECORDING MIGRATORY ORIENTATION OF CAPTIVE BIRDS , 1966 .

[58]  L. Essen,et al.  Cellular Metabolites Enhance the Light Sensitivity of Arabidopsis Cryptochrome through Alternate Electron Transfer PathwaysC , 2014 .

[59]  E. Batschelet Circular statistics in biology , 1981 .