Microbial nanowires with genetically modified peptide ligands to sustainably fabricate electronic sensing devices

Lekbach, Yassir; Ueki, Toshiyuki; Liu, Xiaomeng; Woodard, Trevor L.; Yao, Jianing; Lovley, Derek R.

doi:10.1016/j.bios.2023.115147

Cited by 12 publications

(17 citation statements)

References 52 publications

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“…Electrically conductive nanowires comprised of G. sulfurreducens pilin have applications in diversity of electronic devices (Fu et al, 2020, 2021; Guberman‐Pfeffer et al, 2024; Lekbach et al, 2023; Liu, Fu, et al, 2020; Liu, Gao, et al, 2020; Liu, Ueki, et al, 2022; Lovley & Yao, 2021; Smith et al, 2020). Most notably, heterologous expression of the G. sulfurreducens pilin gene in Escherichia coli has enabled precision genetic engineering of pilin‐based nanowire properties to optimize nanowire conductivity and sensitivity and selectivity for electronic sensing applications (Lekbach et al, 2023; Ueki et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Expression of filaments of the Geobacter extracellular cytochrome OmcS in Shewanella oneidensis

Lin,

Ding,

Zhang

et al. 2024

Biotech & Bioengineering

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The physiological role of Geobacter sulfurreducens extracellular cytochrome filaments is a matter of debate and the development of proposed electronic device applications of cytochrome filaments awaits methods for large‐scale cytochrome nanowire production. Functional studies in G. sulfurreducens are stymied by the broad diversity of redox‐active proteins on the outer cell surface and the redundancy and plasticity of extracellular electron transport routes. G. sulfurreducens is a poor chassis for producing cytochrome nanowires for electronics because of its slow, low‐yield, anaerobic growth. Here we report that filaments of the G. sulfurreducens cytochrome OmcS can be heterologously expressed in Shewanella oneidensis. Multiple lines of evidence demonstrated that a strain of S. oneidensis, expressing the G. sulfurreducens OmcS gene on a plasmid, localized OmcS on the outer cell surface. Atomic force microscopy revealed filaments with the unique morphology of OmcS filaments emanating from cells. Electron transfer to OmcS appeared to require a functional outer‐membrane porin‐cytochrome conduit. The results suggest that S. oneidensis, which grows rapidly to high culture densities under aerobic conditions, may be suitable for the development of a chassis for producing cytochrome nanowires for electronics applications and may also be a good model microbe for elucidating cytochrome filament function in anaerobic extracellular electron transfer.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Expression of filaments of the Geobacter extracellular cytochrome OmcS in Shewanella oneidensis

Lin,

Ding,

Zhang

et al. 2024

Biotech & Bioengineering

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“…An Escherichia coli strain expressing the G. sulfurreducens PilA gene produced 3 nm diameter electrically conductive filaments ( 22 ). The PilA gene could be precision-engineered for specific sensing functions by altering the amino acid content encoded in the PilA gene ( 23 ). Heterologous expression of the G. sulfurreducens PilA gene in Pseudomonas aeruginosa ( 24 ) and Shewanella oneidensis ( 25 ) also yielded 3 nm diameter conductive filaments whose properties could be changed by altering the PilA gene sequence.…”

Section: Introductionmentioning

confidence: 99%

Lack of physiological evidence for cytochrome filaments functioning as conduits for extracellular electron transfer

Schwarz,

Alsaqri,

Lekbach

et al. 2024

mBio

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Extracellular cytochrome filaments are proposed to serve as conduits for long-range extracellular electron transfer. The primary functional physiological evidence has been the reported inhibition of Geobacter sulfurreducens Fe(III) oxide reduction when the gene for the filament-forming cytochrome OmcS is deleted. Here we report that the OmcS-deficient strain from that original report reduces Fe(III) oxide as well as the wild-type, as does a triple mutant in which the genes for the other known filament-forming cytochromes were also deleted. The triple cytochrome mutant displayed filaments with the same 3 nm diameter morphology and conductance as those produced by Escherichia coli heterologously expressing the G. sulfurreducens PilA pilin gene. Fe(III) oxide reduction was inhibited when the pilin gene in cytochrome-deficient mutants was modified to yield poorly conductive 3 nm diameter filaments. The results are consistent with the concept that 3 nm diameter electrically conductive pili (e-pili) are required for G. sulfurreducens long-range extracellular electron transfer. In contrast, rigorous physiological functional evidence is lacking for cytochrome filaments serving as conduits for long-range electron transport. IMPORTANCE Unraveling microbial extracellular electron transfer mechanisms has profound implications for environmental processes and advancing biological applications. This study on Geobacter sulfurreducens challenges prevailing beliefs on cytochrome filaments as crucial components thought to facilitate long-range electron transport. The discovery of an OmcS-deficient strain’s unexpected effectiveness in Fe(III) oxide reduction prompted a reevaluation of the key conduits for extracellular electron transfer. By exploring the impact of genetic modifications on G. sulfurreducens ’ performance, this research sheds light on the importance of 3-nm diameter electrically conductive pili in Fe(III) oxide reduction. Reassessing these mechanisms is essential for uncovering the true drivers of extracellular electron transfer in microbial systems, offering insights that could revolutionize applications across diverse fields.

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“…A diversity of electronic devices has been fabricated with thin-films of e-PNs. These include the 'Air-gen', which generates electricity from atmospheric humidity [14], memristor and neuromorphic memory devices [15,16], and sensors [5,17,18]. The e-PNs in these devices are robust, retaining full functionality over months to years [5,14,[17][18][19].…”

Section: Introductionmentioning

confidence: 99%

Incorporating Microbial Pilin-Based Nanowires into a Water-Stable Electronic Polymer Composite

Sonawane,

Chia,

Ueki

et al. 2024

Preprint

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Electrically conductive protein nanowires (e-PNs), microbially produced from a pilin monomer, are a novel, sustainable electronic material that can be genetically tailored for specific functions. e-PNs, expressed withEscherichia coligrown on the biodiesel byproduct glycerol, and mixed with polyvinyl butyral yielded a transparent, electrically conductive water-stable composite.Composite conductivity was adjusted by modifying the e-PN concentration or incorporating e-PNs genetically tuned for different conductivities. Electronic devices in which composites were the sensor component differentially responded to dissolved ammonia over a wide concentration range (1µM-1M). Genetically modifying e-PNs to display an ammonia-binding peptide on their outer surface increased the sensor response to ammonia 10-fold. These results, coupled with the flexibility to design peptides for specific binding of diverse analytes, demonstrate that sustainably produced e-PNs offer the possibility of incorporating multiple sensor components, each specifically designed to detect different analytes with high sensitivity and selectivity, within one small sensor device.

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Microbial nanowires with genetically modified peptide ligands to sustainably fabricate electronic sensing devices

Cited by 12 publications

References 52 publications

Expression of filaments of the Geobacter extracellular cytochrome OmcS in Shewanella oneidensis

Expression of filaments of the Geobacter extracellular cytochrome OmcS in Shewanella oneidensis

Lack of physiological evidence for cytochrome filaments functioning as conduits for extracellular electron transfer

Incorporating Microbial Pilin-Based Nanowires into a Water-Stable Electronic Polymer Composite

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