Spin-Dependent Electron Transport through Bacterial Cell Surface Multiheme Electron Conduits

This study demonstrates that electron transport through the extracellular multiheme cytochrome conduits (MtrF and OmcA) of *Shewanella oneidensis* MR-1 is spin-selective, suggesting that chiral-induced spin selectivity plays a key role in biotic-abiotic electron transfer processes.

The Gist

Imagine a tiny bacterium, Shewanella oneidensis, living in a muddy environment where it can't breathe oxygen like we do. To survive, it needs to "breathe" solid rocks (minerals) instead. To do this, it has built a biological extension cord made of special proteins called cytochromes. These proteins act like a long-distance wire, carrying electricity from inside the cell to the outside world.

For a long time, scientists knew these wires were efficient, but they didn't know how the electricity moved so well. This new study discovered a hidden feature: these biological wires don't just carry electricity; they also act like spin filters.

Here is the breakdown of what the researchers found, using simple analogies:

1. The "Chiral Highway" (The CISS Effect)

Think of the proteins as a spiral staircase or a corkscrew. In the world of physics, there is a rule called Chiral Induced Spin Selectivity (CISS). It's like a turnstile at a subway station that only lets people through if they are holding their right hand up.

In these bacteria, the "people" are electrons. Because the protein wires are shaped like a spiral (chiral), they force the electrons to spin in a specific direction as they travel. If the electron spins the "wrong" way, it gets blocked or slowed down. This makes the flow of electricity much more efficient because it prevents the electrons from bouncing back (backscattering).

2. The Experiment: The Magnetic Test

The scientists wanted to prove this "spin filter" theory. They set up a clever experiment:

• The Setup: They took two specific protein wires from the bacteria, named MtrF and OmcA, and stuck them onto a magnetic surface (like a tiny magnet).
• The Test: They sent an electric current through these proteins while flipping the magnetic surface upside down (switching the North pole from pointing up to pointing down).
• The Result: When the magnet pointed one way, the electricity flowed easily. When they flipped the magnet, the flow changed significantly.

This proved that the proteins are indeed sensitive to the direction of the electron's spin. It's like finding out that a door only opens easily if you push it with your right hand, but is very hard to open with your left.

3. The Two Wires: MtrF vs. OmcA

The study compared two different protein wires:

• OmcA was the "super-filter." It showed a very strong spin preference (about 63% of the electrons were filtered to spin one way).
• MtrF was also a filter, but a weaker one (about 37%).

Why the difference?
The researchers looked at the "architecture" of these proteins. They found that OmcA has more spiral structures (alpha-helices) wrapped around its core than MtrF. It seems that the more "spiral" the protein is, the better it is at filtering the electron spins.

4. The Importance of Shape

To be sure it was the shape causing this, the scientists "cooked" the proteins (heated them up) to unravel their spiral shapes. Once the proteins lost their spiral structure, the spin-filtering effect disappeared completely. This confirmed that the spiral shape is the key to the magic.

5. Why This Matters (According to the Paper)

The paper suggests this discovery changes how we understand the connection between living cells and non-living materials (like rocks or metal electrodes):

• Magnetic Rocks: Since these wires filter spins, the bacteria might interact differently with magnetic rocks depending on the rock's magnetic field.
• Bio-batteries: This could explain why some experiments show that adding magnets to "microbial fuel cells" (batteries powered by bacteria) makes them work better. The magnet might be helping align the electron spins, making the "wire" more efficient.

In short: The bacteria use spiral-shaped protein wires to transport electricity. These wires act like a spin-selective filter, allowing only electrons with a specific "spin" to pass through efficiently. This discovery adds a new layer of understanding to how bacteria talk to the non-living world around them.

Technical Summary

Technical Summary: Spin-Dependent Electron Transport through Bacterial Cell Surface Multiheme Electron Conduits

Problem Statement
Extracellular electron transfer (EET) is a critical biological process where metal-reducing bacteria, such as Shewanella oneidensis MR-1, respire solid redox-active minerals or interface with electrodes. This process relies on multiheme cytochromes (MHCs), specifically the decaheme proteins MtrF and OmcA, which act as long-distance electron conduits. While previous research has established the high efficiency and rapid electron hopping rates of these proteins, the role of electron spin in this transport has remained uninvestigated. Recent studies on other biomolecules (DNA, oligopeptides) have demonstrated Chiral Induced Spin Selectivity (CISS), where the chiral nature of a molecule couples electron spin to linear momentum, enhancing transmission probability for a specific spin state. The authors hypothesized that this spin-selective phenomenon also governs electron transport through bacterial MHCs, potentially influencing biotic-abiotic interactions and explaining observed magnetic field effects on microbial fuel cell performance.

Methodology
To test the hypothesis of spin selectivity in MtrF and OmcA, the authors employed three distinct experimental approaches, utilizing techniques previously validated for CISS in other chiral systems:

1. Magnetic Conductive Probe Atomic Force Microscopy (mCP-AFM): Solvent-free monolayers of MtrF and OmcA were covalently immobilized via C-terminal tetra-cysteine tags onto a ferromagnetic Nickel (Ni) substrate coated with a thin Gold (Au) layer. A non-magnetic Platinum (Pt) tip served as the top electrode. Current-voltage (I-V) characteristics were measured while the magnetic field of the Ni substrate was oriented with the North pole either "UP" or "DOWN" to alter the spin alignment of the injected electrons.
2. Hall Voltage Measurements: A GaN/AlGaN two-dimensional electron gas Hall device, coated with a thin Au film, was used to detect spin polarization in solution. Protein monolayers were adsorbed onto the device, and a gate voltage was applied to induce charge polarization perpendicular to the monolayer. If accompanied by spin polarization, a transverse Hall voltage would be generated.
3. Spin-Dependent Electrochemistry: Cyclic voltammetry (CV) was performed in a three-electrode cell with the Hall device serving as the working electrode. Simultaneously, the Hall potential was monitored to detect spin selectivity associated with electron transfer through the proteins.

Control experiments included verifying protein immobilization via liquid tapping mode AFM and polarization modulation-infrared reflection-absorption spectroscopy (PM-IRRAS). Crucially, denaturation experiments were conducted by heating proteins to 80°C to assess the dependence of spin selectivity on secondary and tertiary structure.

Key Results

• Spin Selectivity in mCP-AFM: Both MtrF and OmcA exhibited clear spin selectivity. Conductivity was significantly higher when the magnetic field pointed "UP" compared to "DOWN." At a 2.0 V bias, OmcA displayed a spin polarization (SP) of 63 ± 2%, while MtrF showed 37 ± 3%.
• Hall Voltage Correlation: Hall voltage measurements confirmed that spin polarization accompanies field-induced charge polarization in both proteins. The Hall signal scaled linearly with the applied gate voltage. Consistent with mCP-AFM results, OmcA exhibited a larger Hall signal (higher spin polarizability) than MtrF. At 10 V, the OmcA signal corresponded to an effective magnetic field of approximately 200 Gauss.
• Electrochemical Confirmation: Spin-dependent electrochemistry revealed simultaneous Hall signals during cyclic voltammetry, indicating spin selectivity during electron transfer. Notably, the Hall signals did not correlate with the redox peaks of the hemes themselves, suggesting the selectivity arises from conduction through the protein matrix rather than the redox states of the heme centers.
• Structural Dependence: Denaturation of the proteins resulted in a significant decrease in electrochemical current and an order-of-magnitude reduction in the Hall signal, confirming that the native secondary and tertiary structures are essential for the observed spin selectivity.
• Structural Analysis: While MtrF and OmcA have similar overall dimensions and conductivities, OmcA possesses a significantly higher $\alpha$-helical content (18%) compared to MtrF (11%), particularly in the heme-containing domains. The authors suggest this difference in secondary structure surrounding the electron-carrying heme chains may explain the higher spin selectivity in OmcA.

Significance and Claims
The paper establishes that electron transport through the extracellular decaheme cytochromes MtrF and OmcA is spin-selective, governed by the CISS effect. The authors claim this finding:

• Provides a concrete mechanism for understanding how spin-dependent interactions and magnetic fields may control electron transport across biotic-abiotic interfaces.
• Offers a potential explanation for previously reported enhancements in microbial fuel cell performance under specific static magnetic fields, moving beyond previous tentative assignments to oxidative stress or magnetohydrodynamic effects.
• Suggests that spin selectivity may impose constraints on interactions with other chiral molecules (e.g., electron shuttles like flavins) or magnetic minerals (e.g., iron oxides).
• Introduces electron spin as an additional degree of freedom for controlling charge transport in both natural biological systems and biotechnological applications such as bioelectronics and electrosynthesis.

The study does not claim to fully resolve the theoretical basis of CISS in these specific proteins but demonstrates that the phenomenon is robustly present in functional bacterial electron conduits and is dependent on the protein's structural integrity.