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

Multiheme cytochromes, located on the bacterial cell surface, function as long-distance (> 10 nm) electron conduits linking intracellular reactions to external surfaces. This extracellular electron transfer process, which allows microorganisms to gain energy by respiring solid redox-active minerals, also facilitates the wiring of cells to electrodes. While recent studies suggested that a chiral induced spin selectivity effect is linked to efficient electron transmission through biomolecules, this phenomenon has not been investigated in the extracellular electron conduits. Using magnetic conductive probe atomic force microscopy, Hall voltage measurements, and spin-dependent electrochemistry of the decaheme cytochromes MtrF and OmcA from the metal-reducing bacterium <i>Shewanella oneidensis</i> MR-1, we show that electron transport through these extracellular conduits is spin-selective. Our study has implications for understanding how spin-dependent interactions and magnetic fields may control electron transport across biotic-abiotic interfaces in both natural and biotechnological systems.

Download Full-text

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

Journal of the American Chemical Society ◽

10.1021/jacs.9b09262 ◽

2019 ◽

Vol 141 (49) ◽

pp. 19198-19202 ◽

Cited By ~ 8

Author(s):

Suryakant Mishra ◽

Sahand Pirbadian ◽

Amit Kumar Mondal ◽

Mohamed Y. El-Naggar ◽

Ron Naaman

Keyword(s):

Electron Transport ◽

Cell Surface ◽

Bacterial Cell ◽

Bacterial Cell Surface

Download Full-text

Comparison of Atomic Force Microscopy Interaction Forces between Bacteria and Silicon Nitride Substrata for Three Commonly Used Immobilization Methods

Applied and Environmental Microbiology ◽

10.1128/aem.70.9.5441-5446.2004 ◽

2004 ◽

Vol 70 (9) ◽

pp. 5441-5446 ◽

Cited By ~ 91

Author(s):

Virginia Vadillo-Rodríguez ◽

Henk J. Busscher ◽

Willem Norde ◽

Joop de Vries ◽

René J. B. Dijkstra ◽

...

Keyword(s):

Atomic Force Microscopy ◽

Silicon Nitride ◽

Cell Surface ◽

Bacterial Cell ◽

Physical Adsorption ◽

Bacterial Cells ◽

Interaction Forces ◽

Force Microscopy ◽

Bacterial Cell Surface ◽

Atomic Force

ABSTRACT Atomic force microscopy (AFM) has emerged as a powerful technique for mapping the surface morphology of biological specimens, including bacterial cells. Besides creating topographic images, AFM enables us to probe both physicochemical and mechanical properties of bacterial cell surfaces on a nanometer scale. For AFM, bacterial cells need to be firmly anchored to a substratum surface in order to withstand the friction forces from the silicon nitride tip. Different strategies for the immobilization of bacteria have been described in the literature. This paper compares AFM interaction forces obtained between Klebsiella terrigena and silicon nitride for three commonly used immobilization methods, i.e., mechanical trapping of bacteria in membrane filters, physical adsorption of negatively charged bacteria to a positively charged surface, and glutaraldehyde fixation of bacteria to the tip of the microscope. We have shown that different sample preparation techniques give rise to dissimilar interaction forces. Indeed, the physical adsorption of bacterial cells on modified substrata may promote structural rearrangements in bacterial cell surface structures, while glutaraldehyde treatment was shown to induce physicochemical and mechanical changes on bacterial cell surface properties. In general, mechanical trapping of single bacterial cells in filters appears to be the most reliable method for immobilization.

Download Full-text

Single molecule tracking of bacterial cell surface cytochromes reveals dynamics that impact long-distance electron transport

10.1101/2021.11.02.466829 ◽

2021 ◽

Author(s):

Grace W Chong ◽

Sahand Pirbadian ◽

Yunke Zhao ◽

Lori A Zacharoff ◽

Fabien Pinaud ◽

...

Keyword(s):

Electron Transport ◽

Quantum Dot ◽

Single Molecule ◽

Shewanella Oneidensis ◽

Single Particle Tracking ◽

Extracellular Electron Transfer ◽

Long Distance ◽

Electron Hopping ◽

Diffusive Dynamics

Using a series of multiheme cytochromes, the metal-reducing bacterium Shewanella oneidensis MR-1 can perform extracellular electron transfer (EET) to respire redox-active surfaces, including minerals and electrodes outside the cell. While the role of multiheme cytochromes in transporting electrons across the cell wall is well established, these cytochromes were also recently found to facilitate long-distance (micrometer-scale) redox conduction along outer membranes and across multiple cells bridging electrodes. Recent studies proposed that long-distance conduction arises from the interplay of electron hopping and cytochrome diffusion, which allows collisions and electron exchange between cytochromes along membranes. However, the diffusive dynamics of the multiheme cytochromes have never been observed or quantified in vivo, making it difficult to assess their hypothesized contribution to the collision-exchange mechanism. Here we use quantum dot labeling, total internal reflection fluorescence microscopy, and single-particle tracking to quantify the lateral diffusive dynamics of the outer membrane-associated decaheme cytochromes MtrC and OmcA, two key components of EET in S. oneidensis. We observe confined diffusion behavior for both quantum dot-labeled MtrC and OmcA along cell surfaces (diffusion coefficients DMtrC = 0.0192 ± 0.0018 μm2/s, DOmcA = 0.0125 ± 0.0024 μm2/s) and the membrane extensions thought to function as bacterial nanowires. We find that these dynamics can trace a path for electron transport via overlap of cytochrome trajectories, consistent with the long-distance conduction mechanism. The measured dynamics inform kinetic Monte Carlo simulations that combine direct electron hopping and redox molecule diffusion, revealing significant electron transport rates along cells and membrane nanowires.

Download Full-text

Fe(iii)-complex mediated bacterial cell surface immobilization of eGFP and enzymes

Chemical Communications ◽

10.1039/d1cc01575c ◽

2021 ◽

Author(s):

Lilin Feng ◽

Liang Gao ◽

Daniel F. Sauer ◽

Yu Ji ◽

Haiyang Cui ◽

...

Keyword(s):

Cell Surface ◽

Bacterial Cell ◽

Surface Immobilization ◽

E Coli ◽

Bacterial Cell Surface ◽

Reversible Method

A facile and reversible method to immobilize His6-tagged proteins on the E. coli cell surface through the formation of an Fe(iii)-complex.

Download Full-text

Partitioning of phenanthrene into surfactant hemi-micelles on the bacterial cell surface and implications for surfactant-enhanced biodegradation

Water Research ◽

10.1016/j.watres.2013.04.062 ◽

2013 ◽

Vol 47 (13) ◽

pp. 4612-4620 ◽

Cited By ~ 20

Author(s):

Jacquelyn B. Lanzon ◽

Derick G. Brown

Keyword(s):

Cell Surface ◽

Bacterial Cell ◽

Bacterial Cell Surface ◽

Enhanced Biodegradation

Download Full-text

Facile method to stain the bacterial cell surface for super-resolution fluorescence microscopy

The Analyst ◽

10.1039/c4an00574k ◽

2014 ◽

Vol 139 (12) ◽

pp. 3174-3178 ◽

Cited By ~ 16

Author(s):

Ian L. Gunsolus ◽

Dehong Hu ◽

Cosmin Mihai ◽

Samuel E. Lohse ◽

Chang-soo Lee ◽

...

Keyword(s):

Fluorescence Microscopy ◽

Cell Surface ◽

Bacterial Cell ◽

Super Resolution ◽

Bacterial Cell Surface

Download Full-text

Long-distance electron transfer in a filamentous Gram-positive bacterium

Nature Communications ◽

10.1038/s41467-021-21709-z ◽

2021 ◽

Vol 12 (1) ◽

Author(s):

Yonggang Yang ◽

Zegao Wang ◽

Cuifen Gan ◽

Lasse Hyldgaard Klausen ◽

Robin Bonné ◽

...

Keyword(s):

Electron Transfer ◽

Microbial Fuel Cells ◽

Extracellular Electron Transfer ◽

Gram Negative Bacteria ◽

Positive Bacterium ◽

Long Distance ◽

Gram Positive ◽

Gram Negative ◽

Force Microscopy ◽

Cell Envelopes

AbstractLong-distance extracellular electron transfer has been observed in Gram-negative bacteria and plays roles in both natural and engineering processes. The electron transfer can be mediated by conductive protein appendages (in short unicellular bacteria such as Geobacter species) or by conductive cell envelopes (in filamentous multicellular cable bacteria). Here we show that Lysinibacillus varians GY32, a filamentous unicellular Gram-positive bacterium, is capable of bidirectional extracellular electron transfer. In microbial fuel cells, L. varians can form centimetre-range conductive cellular networks and, when grown on graphite electrodes, the cells can reach a remarkable length of 1.08 mm. Atomic force microscopy and microelectrode analyses suggest that the conductivity is linked to pili-like protein appendages. Our results show that long-distance electron transfer is not limited to Gram-negative bacteria.

Download Full-text