Dead vs Alive Quantum Biology: Magnetoreception Enabled via Non-Markovianity

Lead Research Organisation: UNIVERSITY OF EXETER
Department Name: Physics and Astronomy

Abstract

The emerging field of quantum biology suggests that nature may utilise non-trivial quantum effects to realize a classically unattainable advantage in the complex systems of life.
The avian compass, which allows migratory birds to navigate over vast distances, is thought to be a prime example where quantum effects underpin biology. Evidence implies that this sense originates from a light-activated chemical reaction taking place in a protein called cryptochrome, located in the bird's eye. The reaction initiates magnetic field sensitive dynamics of spins, an intrinsic quantum property, of electrons and magnetic nuclei in two "radical" molecules. Consequently, the recombination of the radical pair to reform the protein's resting state is thought to acquire magnetic field sensitivity. However, many open questions remain to be solved to understand the exquisite, possibly quantum enhanced, sensitivity of nature and unlock its design principles.
The majority of current models of the avian compass treat the dynamics of the cryptochrome in isolation. However, recent studies show that the response of an isolated cryptochrome to weak magnetic fields is likely insufficient to support bird navigation. We suggest that the key to this 'interaction strength gap' can be found in the protein's environment. Specifically, we propose that the oft-neglected openness of the spin system to the strongly coupled structured environment can provide an essential sensitivity boost through driving and noise contributions, caused by the physiological motion of the protein at timescales relevant to magnetoreception, and mediated via inter-radical interactions. This enhancement principle contrasts with common efforts to reduce environment interaction, which is seen as detrimental, in most instances of man-made quantum technology. However, for magnetoreception, our preliminary results suggest that, counterintuitively, the environment itself may be utilized to reinforce and revive quantum dynamics - in particular if the interaction with the environment has a finite memory time (non-Markovianity).
We will develop new theory and computationally tractable approaches to unlock the potential of non-Markovian spin dynamics driven by environmental coupling, and to systematically assess the large complex systems of radical-pairs of biology. We will employ wave-function-based methodology in tandem with high-performance and GPU computing techniques to simulate a never before accessible regime that will elucidate non-Markovian enhanced magnetic field sensitivity for realistic systems. Our efforts will culminate in a general, user-friendly software package enabling complex spin dynamics simulations for the scientific community. Our derived insight will supersede current theoretical studies that are oversimplified and resolve the dilemma that current experiments on cryptochrome outside of its biological setting predict inadequate magnetic field sensitivity, thereby opening a new paradigm for biological magnetosensitivity.
This interdisciplinary research program will not only invite a "live" treatment of quantum biology by highlighting a functional role of the living system environment, but also provide essential understanding of spin dynamics ubiquitous in chemistry. Several of these potentially magnetic field sensitive chemical reactions could have implications in biology and health (e.g. neurogenesis, lipid peroxidation), motivating a reassessment of exposure guidelines, and generating tools to control reactions in novel medical treatments. Furthermore, by learning from nature and improving upon it, design principles may be found for condensed phase technology manipulating quantum effects, such as quantum sensors that utilize noise as a resource. This will be addressed in the present research project by developing non-Markovian open quantum system treatments of radical reactions accounting for radical motion and complexity, facilitated by advanced numerical approaches.

Publications

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Agarwal S (2023) The Biological Qubit: Calcium Phosphate Dimers, Not Trimers in The Journal of Physical Chemistry Letters

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Deviers J (2024) Avian cryptochrome 4 binds superoxide. in Computational and structural biotechnology journal

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Gerhards L (2023) Modeling spin relaxation in complex radical systems using MolSpin. in Journal of computational chemistry

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Grüning G (2024) The Effect of Spin Relaxation on Magnetic Compass Sensitivity in ErCry4a. in Chemphyschem : a European journal of chemical physics and physical chemistry

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Schuhmann F (2024) Structural Rearrangements of Pigeon Cryptochrome 4 Undergoing a Complete Redox Cycle. in The journal of physical chemistry. B

 
Description Three, not two, radicals: Revealing the true mechanism of cryptochrome magneto-sensation
Amount £196,000 (GBP)
Funding ID BB/Y51312X/1 
Organisation Biotechnology and Biological Sciences Research Council (BBSRC) 
Sector Public
Country United Kingdom
Start 01/2024 
End 12/2024
 
Title Superoxide magnetosensitivity 
Description We have suggested a hitherto unknown mechanism to explain the cryptic magnetosensitivity of superoxide-containing radical pairs, which has frequently been postulated, but contradicted the convention model, the radical pair model, as a result of too fast spin relaxation. The new model overcomes this conceptual issue by combining the quantum Zeno effect and superoxide-protein interactions that reduce the anions rotational tumbling. The model can rationalize many so far inexplicable observations in the literature and is relevant to the assessment of potential health risks and benefits associated with the exposure to magnetic fields. 
Type Of Material Computer model/algorithm 
Year Produced 2023 
Provided To Others? Yes  
Impact New models and understanding of the effects of exposing biological systems to weak magnetic fields or hypomagnetic fields, which have a potential to revolutionize the use of magnetic fields in medical therapy and are relevant to risk assessment. 
 
Description Collaboration with Manchester, Leicester and NPL on cryptochrome CTT 
Organisation National Physical Laboratory
Country United Kingdom 
Sector Academic/University 
PI Contribution We have contributed molecular dynamics simulations in an effort to explain magnetic field effects in D. melanogaster that are surprisingly mediated by the 54 -residue C-terminal appendix of cryptochrome. We build a model that focuses on the binding of free FAD and predicted the effect of specific mutations of the pedide, which were later confirmed in in vitro experiments.
Collaborator Contribution Our partner have discovered the surprising effect of the C-terminal tail. They have extensively studied the phenomenon through in vivo and in vitro asseyes.
Impact WE are in the processes of acquiring funding for a large-scale joint project, whereby the group would contribute the modelling and interpretation part, employing molecular dynamics and spin dynamics calculations.
Start Year 2023
 
Description Collaboration with Manchester, Leicester and NPL on cryptochrome CTT 
Organisation University of Leicester
Country United Kingdom 
Sector Academic/University 
PI Contribution We have contributed molecular dynamics simulations in an effort to explain magnetic field effects in D. melanogaster that are surprisingly mediated by the 54 -residue C-terminal appendix of cryptochrome. We build a model that focuses on the binding of free FAD and predicted the effect of specific mutations of the pedide, which were later confirmed in in vitro experiments.
Collaborator Contribution Our partner have discovered the surprising effect of the C-terminal tail. They have extensively studied the phenomenon through in vivo and in vitro asseyes.
Impact WE are in the processes of acquiring funding for a large-scale joint project, whereby the group would contribute the modelling and interpretation part, employing molecular dynamics and spin dynamics calculations.
Start Year 2023
 
Description Collaboration with Manchester, Leicester and NPL on cryptochrome CTT 
Organisation University of Manchester
Country United Kingdom 
Sector Academic/University 
PI Contribution We have contributed molecular dynamics simulations in an effort to explain magnetic field effects in D. melanogaster that are surprisingly mediated by the 54 -residue C-terminal appendix of cryptochrome. We build a model that focuses on the binding of free FAD and predicted the effect of specific mutations of the pedide, which were later confirmed in in vitro experiments.
Collaborator Contribution Our partner have discovered the surprising effect of the C-terminal tail. They have extensively studied the phenomenon through in vivo and in vitro asseyes.
Impact WE are in the processes of acquiring funding for a large-scale joint project, whereby the group would contribute the modelling and interpretation part, employing molecular dynamics and spin dynamics calculations.
Start Year 2023
 
Description British Science Festival 2023 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact Showcase of Magnetoreception and Quantum Biology at the British Science Festival held at Exeter's city centre: We informed an audience of the general public about Quantum Biology and its relevance to magnetoreception in birds. The exhibition contained a VR-element, allowing participants to immerse themselves in a bird flight and perceiving, from an bird's eye view, visual magnetoreception in the form of visual modulation patterns. We also provided VR-animations of the protein dynamics that underpin magnetoreception on the molecular level.
Year(s) Of Engagement Activity 2023
URL https://britishsciencefestival.org/programme-2023-revealed/