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Microbial extracellular electron transfer (EET) drives various globally-important environmental phenomena and has biotechnology applications. Diverse prokaryotes have been proposed to perform EET via surface-displayed “nanowires” composed of multi-heme cytochromes. However, the mechanism that enables only a few cytochromes to polymerize into nanowires is unclear. Here, we identify a highly-conserved omcS-companion (osc) cluster that drives the formation of OmcS cytochrome nanowires in Geobacter sulfurreducens. Through a combination of genetic, biochemical, and biophysical methods, we establish that prolyl isomerase-containing chaperon OscH, channel-like OscEFG, and β-propeller-like OscD are involved in the folding, secretion, and morphology maintenance of OmcS nanowires, respectively. OscH and OscG can interact with OmcS. Furthermore, overexpression of oscG accelerates EET by overproducing nanowires in an ATP-dependent manner. Heme loading splits OscD and ΔoscD accelerates cell growth with bundling nanowires. Our findings establish the mechanism and prevalence of a specialized and modular assembly system for nanowires across phylogenetically-diverse species and environmentsmore » « lessFree, publicly-accessible full text available January 15, 2026
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Abstract Microbial respiration via extracellular electron transfer (EET) drives several globally-important environmental processes and has applications in bioenergy, bioremediation, and bioelectronics.
Geobacter sulfurreducens produce micrometer-long cytochrome nanowires for long-range (>10 µm) EET, but also require transmembrane porin-cytochrome complexes (PCCs), which can only perform EET on the cell surface. It was unknown why cells performing long-range EET need both PCCs and nanowires. Using Om(abc)B and OmcS as a model PCC and nanowire, respectively, for EET to Fe(III), we show that PCCs and nanowires form sequential, independent EET pathways where PCCs first kickstart EET and provide energy crucial for nanowire synthesis, and then nanowires perform long-range EET. Our model explains why both PCCs and nanowires are necessary. To understand the underlying EET mechanism, we purified native Om(ab)B and OmcB and found high excitonic coupling among hemes. Their midpoint reduction potentials (-182, -167 mV, respectively) are tuned for efficient electron transport. Additionally, OmcB transfers electrons to Fe(III) ~5 times more efficiently than OmcS. Our work suggests that the metabolic trade-off between PCCs and nanowires results from efficient proteome allocation. Notably, PCCs are widespread in environmentally-important bacteria and co-evolved with OmcS nanowires. This previously-undescribed nanowire synthesis strategy could accelerate EET in diverse microbes and environments.Free, publicly-accessible full text available November 21, 2025 -
Abstract Mixed electronic-ionic conductors are crucial for various technologies, including harvesting power from humidity in a durable, self-sustainable, manner unrestricted by location or environment1,2. Biological proteins have been proposed as mixed conductors for 50 years3,4. Recently,
Geobacter sulfurreducens pili filaments have been claimed to act as nanowires to generate power5,6. Here, we show that the power is generated byG. sulfurreducens -produced cytochrome OmcZ nanowires that show 20,000-fold higher electron conductivity than pili7. Remarkably, nanowires show ultrahigh electron and proton mobility (>0.25 cm2/Vs), owing to directional charge migration through seamlessly-stacked hemes and a charged, hydrogen-bonding surface, respectively. AC impedance spectroscopy and DC conductivity measurements using four-probe van der Pauw and back-gated field-effect-transistor devices reveal that humidity increases carrier mobility by 30,000-fold. Cooling halves the activation energy, thereby accelerating charge transport. Electrochemical measurements identify the voltage and mobilities required to switch pure electronic conduction to mixed conduction for power generation. The high aspect ratio (1:1000) and hydrophilic nanowire surface captures moisture efficiently to reduce oxygen reversibly, generating large potentials (>0.5 V) necessary to sustain high power. Our studies establish a new class of biologically-synthesized, low-cost and high-performance mixed-conductors and identify key design principles for improving power output using highly-tunable electronic and protein structures.Free, publicly-accessible full text available August 12, 2025 -
Abstract Advances in synthetic biology permit the genetic encoding of synthetic chemistries at monomeric precision, enabling the synthesis of programmable proteins with tunable properties. Bacterial pili serve as an attractive biomaterial for the development of engineered protein materials due to their ability to self-assemble into mechanically robust filaments. However, most biomaterials lack electronic functionality and atomic structures of putative conductive proteins are not known. Here, we engineer high electronic conductivity in pili produced by a genomically-recoded
E. coli strain. Incorporation of tryptophan into pili increased conductivity of individual filaments >80-fold. Computationally-guided ordering of the pili into nanostructures increased conductivity 5-fold compared to unordered pili networks. Site-specific conjugation of pili with gold nanoparticles, facilitated by incorporating the nonstandard amino acid propargyloxy-phenylalanine, increased filament conductivity ~170-fold. This work demonstrates the sequence-defined production of highly-conductive protein nanowires and hybrid organic-inorganic biomaterials with genetically-programmable electronic functionalities not accessible in nature or through chemical-based synthesis.