Quantum Biology of Magnetoreception

Quantum Biology of Magnetoreception

Seminar author:Nathan S. Babcock

Event date and time:03/05/2019 02:30:pm

Event location:GIQ Seminar Room (C5/262)

Event contact:N.S.Babcock@exeter.ac.uk

Despite an established consensus that many forms of life can reliably detect the Earth’s weak magnetic field, it is unclear how many complex organisms sense it [1]. Most prominent mechanistic proposals invoke a quantum-biological model [2], relying on the assumption that an excitonic “radical” electron pair [3] facilitates magnetoreception of the Earth’s field (50 μT).

Field-dependent decay products of this spin-crossing reaction are believed to constitute a decoherence channel to a signaling state that discriminates the field angle and inclination, yet essential details of the scheme are lacking. Comprehensive models of requisite activation [4-6], charge separation [7-8], chemical amplification [9-10], anisotropic response [11], coherence-preserving [12] and/or decoherence-limiting [13] steps are needed. Given the rich complexity of the biological milieu and lacking a consistent in vitro model, mechanistic features must be identified empirically in order to confirm a viable magnetic sense receptor.

In this seminar lecture, I review features of competing models of cryptochrome-based magnetoreception, in the context of existing theory and experiment. Seminar content will address recent conflicts [14-17] between evidences and conventional model proposals [18-19]. Implications of these conflicts will be explored in terms of an expanded model that involves the amplification of the spin-chemical effect—with an eye toward broad generalization of existing principles [20-23]. We assess criticism of models reliant on quantum entanglement in a dynamic environment at physiological temperature [24-28]. If time permits, we will discuss overall challenges facing a broad class of reaction schemes that depend upon coherent singlet-triplet interconversion to enable magnetoreception. In closing, we will consider how the engineering of biosynthetic systems [29] could enable new technologies with ramifications for metrology [30], magnetogenetics [31], and medicine [32].

Reference List:

1. Johnsen & Lohmann, “Magnetoreception in animals,” Physics Today 61, 29-35 (2008).

2. Lambert et al., “Quantum biology,” Nature Physics 9, 10-18 (2013).

3. Rodgers & Hore, “Chemical magnetoreception in birds: The radical pair mechanism,” Proceedings of the National Academy of Sciences 106, 353-360 (2009).

4. Nießner, Denzau, Peichl, Wiltschko, & Wiltschko, “Magnetoreception: activation of avian cryptochrome 1a in various light conditions,” Journal of Comparative Physiology A 204, 977-984 (2018).

5. Ahmad, “Photocycle and signaling mechanisms of plant cryptochromes,” Current Opinion in Plant Biology 33, 108-115 (2016).

6. Bouly et al., “Cryptochrome Blue Light Photoreceptors Are Activated through Interconversion of Flavin Redox States” Journal of Biological Chemistry 282, 9383–9391 (2007).

7. Firmino et al., “Quantum effects in ultrafast electron transfers within cryptochromes,” Physical Chemistry Chemical Physics 18, 21442-21457 (2016).

8. Nohr, “Extended Electron-Transfer in Animal Cryptochromes Mediated by a Tetrad of Aromatic Amino Acids,” Biophysical Journal 111, 301-311 (2016).

9. Kattnig et al., “Chemical amplification of magnetic field effects relevant to avian magnetoreception,” Nature Chemistry 8, 384-391 (2016).

10. Kattnig & Hore, “The sensitivity of a radical pair compass magnetoreceptor can be significantly amplified by radical scavengers,” Scientific Reports 7, 11640 (2017).

11. Hiscock et al., “The quantum needle of the avian magnetic compass,” Proceedings of the National Academy of Sciences113, 4634-4639.

12. Hiscock, “Long-lived Spin Coherence in Radical Pair Compass Magnetoreception,” PhD Thesis, University of Oxford (2018).

13. Kattnig, “Radical-Pair-Based Magnetoreception Amplified by Radical Scavenging: Resilience to Spin Relaxation,” Journal of Physical Chemistry B 121, 10215–10227 (2017).

14. Pooam et al., “Magnetic sensitivity mediated by the Arabidopsis blue‐light receptor cryptochrome occurs during flavin reoxidation in the dark,” Planta 249, 319-332 (2019).

15. Agliassa, Narayana, Christie, & Maffei, “Geomagnetic field impacts on cryptochrome and phytochrome signaling,” Journal of Photochemistry & Photobiology B, 185 32-40 (2018).

16. Wiltschko, Ahmad, Nießner, Gehring, & Wiltschko “Light-dependent magnetoreception in birds: the crucial step occurs in the dark,” Royal Society Interface 13, 20151010 (2016).

17. Müller & Ahmad, “Light-activated Cryptochrome Reacts with Molecular Oxygen to Form a Flavin–Superoxide Radical Pair Consistent with Magnetoreception,” Journal of Biological Chemistry 286, 21033–21040 (2011).

18. Hore & Mouritsen, “The Radical Pair Mechanism of Magnetoreception,” Annual Review of Biophysics, 45 299-344 (2016).

19. Wiltschko & Wiltschko, “Sensing Magnetic Directions in Birds: Radical Pair Processes Involving Cryptochrome,” Biosensors 4, 221-242 (2014).

20. Keens, Bedkihal, & Kattnig, “Magnetosensitivity in Dipolarly Coupled Three-Spin Systems,” Physical Review Letters 121, 096001 (2018)

21. Lindoy & Manolopoulos, “Simple and Accurate Method for Central Spin Problems,” Physical Review Letters 120, 220604 (2018).

22. Lewis, Manolopoulos, & Hore, “Asymmetric recombination and electron spin relaxation in the semiclassical theory of radical pair reactions,” Journal of Chemical Physics 141, 044111 (2014).

23. Manolopoulos & Hore, “An improved semiclassical theory of radical pair recombination reactions,” Journal of Chemical Physics 139, 124106 (2013).

24. Gauger & Benjamin, “Comment on ‘Quantum Coherence and Sensitivity of Avian Magnetoreception’,” Physical Review Letters 110, 178901 (2013).

25. Pauls, Zhang, Berman, & Kais, “Quantum coherence and entanglement in the avian compass,” Physical Review E 97, 062704 (2013).

26. Hogben, Biskup, & Hore, “Entanglement and Sources of Magnetic Anisotropy in Radical Pair-Based Avian Magnetoreceptors,” Physical Review Letters 109, 220501 (2012).

27. Bandyopadhyay, Paterek, Kaszlikowski, “Quantum Coherence and Sensitivity of Avian Magnetoreception,” Physical Review Letters 109, 110502 (2012).

28. Mendive-Tapia et al., “Multidimensional Quantum Mechanical Modeling of Electron Transfer and Electronic Coherence in Plant Cryptochromes: The Role of Initial Bath Conditions,” Journal of Physical Chemistry B 122, 126−136 (2017).

29. Bialas et al., “Engineering an Artificial Flavoprotein Magnetosensor,” Journal of the American Chemical Society 138, 16584-16587 (2016).

30. Imamoglu & Whaley, “Photoactivated biological processes as quantum measurements,” Physical Review E 91, 022714 (2015).

31. Meister, “Physical limits to magnetogenetics,” eLife 5, e17210 (2016).

32. Juutilainen, Herrala, Luukkonen, Naarala, & Hore, “Magnetocarcinogenesis: is there a mechanism for carcinogenic effects of weak magnetic fields?” Proceedings of the Royal Society B 285, 20180590 (2018).