Direct Extracellular Electron Transfer of the Geobacter sulfurreducens Pili Relevant to Interaromatic Distances

Abstract

Microorganisms can transfer electrons directly to extracellular acceptors, during which organic compounds are oxidized to carbon dioxide. One of these microbes, Geobacter sulfurreducens, is well known for the “metallic-like” conductivity of its type IV pili. However, there is no consensus on what the mechanism for electron transfer along these conductive pili is. Based on the aromatic distances and orientations of our predicted models, the mechanism of electron transfer in the Geobacter sulfurreducens (GS) pili was explored by quantum chemical calculations with Marcus theory of electron transfer reactions. Three aromatic residues from the N-terminal α-helix of the GS pilin subunit are packed together, resulting in a continuous pi-pi interaction chain. The theoretical conductance (4.69 μS/3.85 μS) of the predicted models is very similar to that in the experiments reported recently (3.40 μS). These findings offer a new concept that the GS pili belongs to a new class of proteins that can transport electrons through pi-pi interaction between aromatic residues and also provide a valuable tool for guiding further researches of these conductive pili, to investigate their roles in biogeochemical cycling, and potential applications in biomaterials, bioelectronics, and bioenergy.

Spatially Resolved Electron Transport through Anode‐Respiring Geobacter sulfurreducens Biofilms: Controls and Constraints

“…Simply manipulating the value of φ c does not lead to activity patterns consistent with observational data. This [66,116] D cyt m 2 s À 1 10 À 5 -10 À 10 (7 × 10 À 7 ) Effective diffusion coefficient Estimated from [116][117][118] A act m 2 10 À 14 -10 À 13 Redox active surface area Estimated from [108] β -0.5 Charge transfer coefficient [108] φ anode V À 0.1, + 0.24 Poised low, high anode potential [58] φ ox/red 0' V À 0.07, À 0.15 Redox-active center mid-potential [44,56] N nw,cell -1-200 (49) Number of connections per cell Estimated from [32,[108][109][110][111] Fixed concentration were imposed for all chemical species at the outer domain boundary except for CO is due to the fact that lowering biofilm resistance also increases cell activity, as a result of reduced potential loss (Figure S12C) and increased usable electric potential (φ net ) (Figure S12B). In addition, pH also further decreases near the electrode as a result of increased cell activity (Figure S12D).…”

“…Dcyt m 2 s -1 10 -5 -10 -10 (7×10 -7 ) Effective diffusion coefficient Estimated from [116][117][118] kD m 4 mol s -1 10 -5 -10 5 (100) Electron transfer rate constant Estimated from Dcyt = kD[Cyttot]δ δ nm 0.7 Spatial distance between adjacent redox-active molecules [119] σ S m -1 10 -4 -10 -2 (1.5×10 -3 ) Biofilm conductivity [12,21,35,120] Anw m 2 1.26×10 -17 Cross-section area of a single pilus Calculated from dnw dnw nm 4 Diameter of a single pilus [31,32] Aact m 2 10 -14 -10 -13 Redox active surface area Estimated from [108] β -0.5 Charge transfer coefficient [108] ϕanode V -0.1, +0.24 Poised low, high anode potential [58] ϕox/red 0' V -0.07, -0.15 Redox-active center mid-potential [44,56] Nnw,cell -1-200 (49) Number of connections per cell Estimated from [32,[108][109][110][111] Fixed concentration were imposed for all chemical species at the outer domain boundary except for CO2, CO3 2-, Cytred, R-COOH, R-NH2, R-PO4H2. No flux conditions were imposed at the bulk-biofilm interface and anode surface for CO2, CO3 2-, Cytred.…”

Atomic and Electronic Structure of Pilus from Geobacter sulfurreducens through QM/MM Calculations: Evidence for Hole Transfer in Aromatic Residues

“…The involvement of aromatic amino acids with the conductive properties of biomolecules has also been a matter of debate. − Studies point to a key role of these amino acids in pilus conductivity, − suggesting that the π–π stacking can contribute to the electron transfer. It is known that amino acids such as tyrosine and tryptophan have the lowest redox potentials among all of the typical amino acids, which can be the determinant factor for charge generation and transport through the hopping mechanism .…”

Spatially Resolved Electron Transport through Anode‐Respiring Geobacter sulfurreducens Biofilms: Controls and Constraints

“…Dcyt m 2 s -1 10 -5 -10 -10 (7×10 -7 ) Effective diffusion coefficient Estimated from [116][117][118] kD m 4 mol s -1 10 -5 -10 5 (100) Electron transfer rate constant Estimated from Dcyt = kD[Cyttot]δ δ nm 0.7 Spatial distance between adjacent redox-active molecules [119] σ S m -1 10 -4 -10 -2 (1.5×10 -3 ) Biofilm conductivity [12,21,35,120] Anw m 2 1.26×10 -17 Cross-section area of a single pilus Calculated from dnw dnw nm 4 Diameter of a single pilus [31,32] Aact m 2 10 -14 -10 -13 Redox active surface area Estimated from [108] β -0.5 Charge transfer coefficient [108] ϕanode V -0.1, +0. 24 Poised low, high anode potential [58] ϕox/red 0' V -0.07, -0.15 Redox-active center mid-potential [44,56] Nnw,cell -1-200 (49) Number of connections per cell Estimated from [32,[108][109][110][111] Fixed concentration were imposed for all chemical species at the outer domain boundary except for CO2, CO3 2-, Cytred, R-COOH, R-NH2, R-PO4H2.…”