Coupling Between Electrons' Spin and Proton Transfer in Chiral Biological Crystals

Physical Chemistry Chemistry Quantum Physics Biophysics Biochemistry Life Sciences Physics
proton transfer electron spin chiral-induced spin selectivity lysozyme crystals proton-coupled electron transfer

Academic Background

Proton transfer plays a central role in biological energy conversion (e.g., ATP synthesis) and signal transduction. Traditional theory posits that protons move via a “hopping mechanism” through water chains or amino acid side chains, while the recently proposed “proton-coupled electron transfer” (PCET) hypothesis suggests that electron transfer may synchronously participate in this process. Given the highly chiral nature of biological systems, the “chiral-induced spin selectivity” (CISS) effect—where electrons exhibit spin polarization when moving through chiral environments—may influence this process. Using lysozyme crystals as a model, this study reveals for the first time the quantum correlation between proton transfer efficiency and electron spin states.

Source of the Paper

The research was conducted by Yossi Paltiel’s team at the Hebrew University of Jerusalem in collaboration with Ben-Gurion University, the Weizmann Institute of Science, and other institutions. It was published in PNAS (May 2025, vol. 122, no. 19). Corresponding authors include Ron Naaman, Nurit Ashkenasy, and Yossi Paltiel.

Research Process and Findings

1. Experimental System Construction

Research Subject:
Hen egg white lysozyme was used to prepare single crystals via the hanging-drop vapor-diffusion method, yielding tetragonal crystals approximately 300 μm in size, with their structure fixed by glutaraldehyde cross-linking.

Innovative Device:
- Designed a micron-scale electrode array (2 μm spacing) with alternating nickel (Ni, ferromagnetic) and gold (Au, non-magnetic) electrodes.
- Applied an 80 mT external magnetic field to control the magnetization direction of Ni electrodes (N-pole up/S-pole up).
- Precisely controlled environmental humidity (60-80% RH) and temperature (23-35°C).

2. Verification of Electron Spin-Dependent Proton Conduction

Key Experiments:
- DC I-V Testing: At 70% humidity, a 20% current difference was observed between N and S magnetization directions in Ni electrodes (Fig. 1d).
- Impedance Spectroscopy: Nyquist plots showed semicircle radii varying with magnetization direction (Fig. 2a). The relaxation time extracted from the equivalent circuit model was three times faster for N polarization (18 ms) than for S polarization (60 ms).
- Isotope Control: The spin effect weakened in a D₂O environment, confirming phonon involvement (Fig. 3c).

Mechanism Validation:
- No significant spin effect was observed in the gold electrode control group (Fig. 1e).
- Second harmonic generation measurements revealed asymmetric heating responses correlated with spin injection direction (Fig. 4c), confirming electron-phonon coupling.

3. Environmental Parameter Modulation

Humidity Effects:
- At 80% humidity, the CISS effect decreased to one-third of its value at 60% (Fig. 3b), as water-mediated proton transfer weakened chiral lattice interactions.
- The effect strengthened at higher temperatures (35°C, Fig. 3d), consistent with phonon-assisted transport theory.

Core Conclusions and Value

Theoretical Breakthroughs

  1. PCET Mechanism Validation: First demonstration in biological crystals that proton transfer efficiency is modulated by electron spin states, supporting the PCET hypothesis.
  2. Chirality-Spin-Phonon Tripartite Coupling: Proposed a new model (Fig. 5)—chiral environments induce electron spin polarization → excite chiral phonons → lower proton transfer energy barriers.
  3. Quantum Biological Significance: Revealed that spin degrees of freedom may participate in quantum mechanisms of energy/information transfer in biological systems.

Application Prospects

  • Biosensors: Design high-sensitivity proton detection devices using spin modulation.
  • Biomimetic Materials: Develop novel proton conductors with chiral phonon coupling.
  • Disease Mechanisms: Provide new insights into diseases involving proton transfer abnormalities, such as mitochondrial dysfunction.

Research Highlights

  1. Methodological Innovations:

    • Hybrid device design combining ferromagnetic electrodes with biological single crystals.
    • Second harmonic measurements visualizing phonon-spin interactions.

  2. Original Discoveries:

    • First extension of the CISS effect to proton transport.
    • Observed weakened effects in D₂O environments (Fig. 3c), providing direct evidence for phonon involvement.

  3. Interdisciplinary Value:

    • Bridged quantum physics (spin polarization), biochemistry (proton transfer), and materials science (chiral crystals).

Supplementary Information

Theoretical Model:
A modified Warburg impedance formula (Equation 1) incorporating spin polarization parameters was proposed for proton mobility calculations, achieving a fitting accuracy of R² > 0.98 (SI Appendix, Fig. S2).

Data Availability:
All raw data are publicly available via PNAS supplementary materials, including:
- 12 sets of impedance spectra under varying humidity conditions.
- I-V curves for five electrode configurations.
- Atomic force microscopy (AFM) data characterizing crystal morphology.