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Explaining the avian compass through sustained quantum dynamics in driven, open three-radical systems

Lead Research Organisation: UNIVERSITY OF EXETER
Department Name: Physics

Abstract

In the past 25 years, we have witnessed the emergence of quantum technologies, including quantum computers or simulators, from a scientific dream to reality. Google's claim to have achieved quantum supremacy has spurred the global race toward harnessing the quantum advantage. The next major advance, enabled by the applications of quantum computers, may become a reality within decades. The breakthrough hinges on one fundamental imperative: the need to sustain quantum superpositions and, crucially, entanglement in noisy environments.

Has nature evolved to exploit quantum phenomena in ways that surpass current technologies? Could truly quantum effects operate in the warm, wet and noisy environment that is characteristic of life? Does this provide a decisive advantage over "classical" processes? Indeed, evidence accumulated over the last four decades does support a conclusion that various organisms employ coherent quantum dynamics to enable magnetoreception: the ability to sense the geomagnetic field.

Yet, it remains to be shown exactly how coherent quantum effects can operate in the warm, wet, and noisy surroundings that are characteristic of biology. Previous studies provided a conceptual model, but failed to rationalize the sustained quantum coherence that is believed to enable this exquisite sensitivity to the magnetic field. We believe this failure is a consequence of an inadequate description of the biological environment, i.e. the openness of the quantum system as it is coupled to the protein motion-a deficit which we here shall overcome. This treatment will explain how living systems could exercise the benefit of a quantum effect to provide a decisive advantage to life. We will do this by focusing, for the first time on systems of radical pairs and three radicals, for which we hope to be able to demonstrate that radical motion can amplify magnetic field effects and sustain quantum dynamics, if the system is driven to a metastable state not accessible in closed-system formulations.

Publications

10 25 50
 
Description The ability of animals to sense the weak Earth's magnetic field (magnetoreception) has long been a mystery. A leading theory, motivated by theoretical and experimental studies, suggests it relies on quantum phenomena taking place in the cryptochrome protein, for example, located in bird's retinae. However, whilst providing the conceptual basis of the mechanism, thus far models have been unable to produce the levels of sensitivity required to agree with ethological observations on magnetic field responses. In this investigation we set out to rationalise how sustained quantum coherence could enable magnetoreception within a radical-based (molecules with an odd number of electrons) compass that relies on the dynamics of quantum spin (an intrinsic angular momentum of electrons and nuclei). Our objective was to go beyond prior idealised studies, that provided a conceptual model yet neglected complexity inherent in biological systems such as interactions between electron spins, and to the many surrounding nuclei and protein.

Surprisingly, as it contrasted the existing understanding based on toy models, we found that an often-used measure of coherence of the electronic system alone was not a good system-independent quantifier of compass sensitivity. Instead, we discovered that global coherence, i.e. of the electronic and nuclear system together, strongly correlated with compass sensitivity across different radical systems, thus justifying its rationalisation as a resource to magnetoreception and furthering our fundamental understanding of quantum coherence in complex systems. The results of this study were published in the journal Scientific Reports entitled "Observations about utilitarian coherence in the avian compass" and featured in its top 100 list of publications in Physics of 2022.

With respect to the second complexity of biological systems, the protein environment, we hypothesised that it could drive motion of the radicals and in turn amplify magnetic effects, for example, by sustaining quantum spin dynamics. Our work allowed us to confirm this hypothesis and demonstrate that harmonically driven radicals can indeed enhance magnetic field sensitivity and restore it despite detrimental inter-radical interactions. We found this motion can alter the systems energies, thereby freeing it when it becomes trapped in a particular state that inhibits sensitivity, by allowing coherent inter-conversion between states to occur via so called driven non-adiabatic transitions (Landau-Zener-Stückelberg-Majorana transitions), a truly quantum phenomena not described by semiclassical theory. The results of this study, published in the letter "Driven Radical Motion Enhances Cryptochrome Magnetoreception: Toward Live Quantum Sensing" in the Journal of Physical Chemistry Letters, has enabled us to revolutionise established radical-based mechanisms of spin chemistry, thereby paving the path to new avenues of discovery that could provide a route towards resolving the sensitivity gap between quantum theory and ethological observation.
Exploitation Route Concerning the development of the quantum theory of magnetoreception, our work has provided deep insights into the necessity of treating the complexity inherent in biological systems and expanding upon the established mechanism. We anticipate that this will motivate the scientific community to revisit the theory and experiments with this in mind, inspiring new research to be conducted that will further our understanding of quantum dynamics in magnetoreception, spin chemistry, and quantum biology in general. Within our own group this has facilitated a collaboration investigating the limits of precision possible, as system complexity is increased, via quantum information studies. Furthermore, it has enabled us to take our findings forward and develop a new theory that suggests that a strongly coupled structured protein environment can provide an essential sensitivity boost through driving components and noise contributions that may be utilized to reinforce and revive quantum dynamics - in particular if the interaction with the environment has a finite memory time (non-Markovianity). This hypothesis invites a description that suggests the quantum processes within a living system (in vivo) may be bolstered by dynamics not present within "dead" systems, e.g. current in vitro system explorations, and is the central concept of the EPSRC grant "Dead vs Alive Quantum Biology: Magnetoreception Enabled via Non-Markovianity." We anticipate that this will lead to a paradigm shift in quantum biology and help to bridge the gap to the open quantum systems community motivating interdisciplinary collaborative studies and methodology development. Our studies could also encourage a route for the control of quantum phenomena both in biological, therapeutic, and technological applications, by understanding how the enhancing effects we have discovered may be produced and engineered.
Sectors Environment

Healthcare

Manufacturing

including Industrial Biotechology

Pharmaceuticals and Medical Biotechnology

Other

 
Description Reported on the potenitial of quantum effects to underpin the putative magnetosensitivity of reactive oxygen species
Geographic Reach Europe 
Policy Influence Type Contribution to a national consultation/review
 
Description Spin biology under optimal quantum control
Amount $611,000 (USD)
Funding ID N62909-21-1-2018 
Organisation ONRG Office of Naval Research Global 
Sector Public
Country United States
Start 08/2021 
End 08/2024
 
Description The quantum avian compass probed on the single molecule level
Amount £200,889 (GBP)
Funding ID EP/X018822/1 
Organisation Engineering and Physical Sciences Research Council (EPSRC) 
Sector Public
Country United Kingdom
Start 11/2022 
End 04/2024
 
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 Collaboration with Prof. Aiello and Banerjee (USLA) 
Organisation University of California, Los Angeles (UCLA)
Country United States 
Sector Academic/University 
PI Contribution We have contributed to this collaboration with spin dynamics calculations, both of radical pair systems, which are at the heart of the "Explaining the avian compass through sustained quantum dynamics in driven, open three-radical systems"-project, and of nuclear spin clusters, i.e. the Posner molecule.
Collaborator Contribution Our partners have contributed ab initio and classical molecular dynamics simulations and DFT calculations.
Impact We have jointly authored a publication in a related field and are currently in the processes of preparing another. The project is multi-disciplinary; it involves the QuBiT Lab and Ab Initio Simulations Lab at the Electrical and Computer Engineering at UCLA and the Living Systems Institute and Department of Physics at the University of Exeter.
Start Year 2021
 
Title CUDA-enabled kernes for spin dynamics calculations 
Description We have develop a CUDA-enabled kernels for the simulation of magnetic field effects as resulting from the spin dynamics in radical pairs. These programs allows solving the Liouville von-Neumann equation of the spin density operator of radical pairs comprising a large number of hyperfine-coupled nuclear spins on GPUs, thereby providing simulations of larger, more realistic systems than was previously achievable. 
Type Of Technology New/Improved Technique/Technology 
Year Produced 2021 
Impact These sets of programs are essential for the realization of this research project, as they provide us with the tools necessary to address more realistic spin systems. The kernels have been partly released to the public domain (as supplemental data of a recent publication). We plan to collect the kernels in a toolkit, expand their scope and optimize the underlying numerical methods. We will then release the toolkit subject to an open source license in the near future. 
 
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/
 
Description VR exhibition on quantum navigation and magnetoreception at the Futures festival 
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 RCoI presented a 2 day VR exhibition to the public at the Futures festival 09/24 in Exeter on quantum navigation and magnetoreception.
Year(s) Of Engagement Activity 2024