An Escherichia coli Chassis for Production of Electrically Conductive Protein Nanowires
- Toshiyuki UekiToshiyuki UekiDepartment of Microbiology, University of Massachusetts-Amherst, Amherst, Massachusetts 01003, United StatesInstitute for Applied Life Sciences, University of Massachusetts-Amherst, Amherst, Massachusetts 01003, United StatesMore by Toshiyuki Ueki
- ,
- David J. F. WalkerDavid J. F. WalkerDepartment of Microbiology, University of Massachusetts-Amherst, Amherst, Massachusetts 01003, United StatesInstitute for Applied Life Sciences, University of Massachusetts-Amherst, Amherst, Massachusetts 01003, United StatesMore by David J. F. Walker
- ,
- Trevor L. WoodardTrevor L. WoodardDepartment of Microbiology, University of Massachusetts-Amherst, Amherst, Massachusetts 01003, United StatesMore by Trevor L. Woodard
- ,
- Kelly P. NevinKelly P. NevinDepartment of Microbiology, University of Massachusetts-Amherst, Amherst, Massachusetts 01003, United StatesMore by Kelly P. Nevin
- ,
- Stephen S. NonnenmannStephen S. NonnenmannInstitute for Applied Life Sciences, University of Massachusetts-Amherst, Amherst, Massachusetts 01003, United StatesDepartment of Mechanical and Industrial Engineering, University of Massachusetts-Amherst, Amherst, Massachusetts 01003, United StatesMore by Stephen S. Nonnenmann
- , and
- Derek R. Lovley*Derek R. Lovley*Email: [email protected]Department of Microbiology, University of Massachusetts-Amherst, Amherst, Massachusetts 01003, United StatesInstitute for Applied Life Sciences, University of Massachusetts-Amherst, Amherst, Massachusetts 01003, United StatesMore by Derek R. Lovley
Abstract

Geobacter sulfurreducens’ pilin-based electrically conductive protein nanowires (e-PNs) are a revolutionary electronic material. They offer novel options for electronic sensing applications and have the remarkable ability to harvest electrical energy from atmospheric humidity. However, technical constraints limit mass cultivation and genetic manipulation of G. sulfurreducens. Therefore, we designed a strain of Escherichia coli to express e-PNs by introducing a plasmid that contained an inducible operon with E. coli genes for type IV pili biogenesis machinery and a synthetic gene designed to yield a peptide monomer that could be assembled into e-PNs. The e-PNs expressed in E. coli and harvested with a simple filtration method had the same diameter (3 nm) and conductance as e-PNs expressed in G. sulfurreducens. These results, coupled with the robustness of E. coli for mass cultivation and the extensive E. coli toolbox for genetic manipulation, greatly expand the opportunities for large-scale fabrication of novel e-PNs.
Cited By
This article is cited by 50 publications.
- Nga T. Lam, Joshua B. McCluskey, Dominic J. Glover. Harnessing the Structural and Functional Diversity of Protein Filaments as Biomaterial Scaffolds. ACS Applied Bio Materials 2022, 5 (10) , 4668-4686. https://doi.org/10.1021/acsabm.2c00275
- Lina J. Bird, Biki B. Kundu, Tanya Tschirhart, Anna D. Corts, Lin Su, Jeffrey A. Gralnick, Caroline M. Ajo-Franklin, Sarah M. Glaven. Engineering Wired Life: Synthetic Biology for Electroactive Bacteria. ACS Synthetic Biology 2021, 10 (11) , 2808-2823. https://doi.org/10.1021/acssynbio.1c00335
- Yun-Lu Sun, Brian J. Montz, Ryan Selhorst, Hai-Yan Tang, Jiaxin Zhu, Kelly P. Nevin, Trevor L. Woodard, Alexander E. Ribbe, Thomas P. Russell, Stephen S. Nonnenmann, Derek R. Lovley, Todd Emrick. Solvent-Induced Assembly of Microbial Protein Nanowires into Superstructured Bundles. Biomacromolecules 2021, 22 (3) , 1305-1311. https://doi.org/10.1021/acs.biomac.0c01790
- Hui Chen, Olja Simoska, Koun Lim, Matteo Grattieri, Mengwei Yuan, Fangyuan Dong, Yoo Seok Lee, Kevin Beaver, Samali Weliwatte, Erin M. Gaffney, Shelley D. Minteer. Fundamentals, Applications, and Future Directions of Bioelectrocatalysis. Chemical Reviews 2020, 120 (23) , 12903-12993. https://doi.org/10.1021/acs.chemrev.0c00472
- Ben Myers, Francesco Catrambone, Stephanie Allen, Phil J. Hill, Katalin Kovacs, Frankie J. Rawson. Engineering nanowires in bacteria to elucidate electron transport structural–functional relationships. Scientific Reports 2023, 13 (1) https://doi.org/10.1038/s41598-023-35553-2
- Lianfu Liang, Qilin Yu, Yang Li, Zhiqiang Zhao, Shengqiang Fan, Yaobin Zhang. Effects of magnetite on nitrate-dependent anaerobic oxidation of methane in an anaerobic membrane biofilm reactor: Metatranscriptomic analysis and mechanism prediction. Environmental Technology & Innovation 2023, 32 , 103288. https://doi.org/10.1016/j.eti.2023.103288
- Yuting Jin, Enze Zhou, Toshiyuki Ueki, Danni Zhang, Yongqiang Fan, Dake Xu, Fuhui Wang, Derek R. Lovley. Accelerated Microbial Corrosion by Magnetite and Electrically Conductive Pili through Direct Fe 0 ‐to‐Microbe Electron Transfer. Angewandte Chemie 2023, 135 (38) https://doi.org/10.1002/ange.202309005
- Yuting Jin, Enze Zhou, Toshiyuki Ueki, Danni Zhang, Yongqiang Fan, Dake Xu, Fuhui Wang, Derek R. Lovley. Accelerated Microbial Corrosion by Magnetite and Electrically Conductive Pili through Direct Fe 0 ‐to‐Microbe Electron Transfer. Angewandte Chemie International Edition 2023, 62 (38) https://doi.org/10.1002/anie.202309005
- Zixuan You, Jianxun Li, Yuxuan Wang, Deguang Wu, Feng Li, Hao Song. Advances in mechanisms and engineering of electroactive biofilms. Biotechnology Advances 2023, 66 , 108170. https://doi.org/10.1016/j.biotechadv.2023.108170
- Joshua M. Lawrence, Rachel M. Egan, Thomas Hoefer, Alberto Scarampi, Linying Shang, Christopher J. Howe, Jenny Z. Zhang. Rewiring photosynthetic electron transport chains for solar energy conversion. Nature Reviews Bioengineering 2023, 1857 https://doi.org/10.1038/s44222-023-00093-x
- Xiaomeng Liu, Hongyan Gao, Lu Sun, Jun Yao. Generic Air‐Gen Effect in Nanoporous Materials for Sustainable Energy Harvesting from Air Humidity. Advanced Materials 2023, https://doi.org/10.1002/adma.202300748
- Yassir Lekbach, Toshiyuki Ueki, Xiaomeng Liu, Trevor Woodard, Jun Yao, Derek R. Lovley. Microbial nanowires with genetically modified peptide ligands to sustainably fabricate electronic sensing devices. Biosensors and Bioelectronics 2023, 226 , 115147. https://doi.org/10.1016/j.bios.2023.115147
- Derek R. Lovley. Response to Wang et al.: evidence contradicting the cytochrome-only model. Trends in Microbiology 2023, 20 https://doi.org/10.1016/j.tim.2023.03.006
- Christopher M. Dundas, Benjamin K. Keitz. Tapping the potential of Gram-positive bacteria for bioelectrochemical applications. Trends in Biotechnology 2023, 41 (3) , 273-275. https://doi.org/10.1016/j.tibtech.2022.12.008
- Joshua T. Atkinson, Marko S. Chavez, Christina M. Niman, Mohamed Y. El‐Naggar. Living electronics: A catalogue of engineered living electronic components. Microbial Biotechnology 2023, 16 (3) , 507-533. https://doi.org/10.1111/1751-7915.14171
- Eric Szmuc, David J.F. Walker, Dmitry Kireev, Deji Akinwande, Derek R. Lovley, Benjamin Keitz, Andrew Ellington. Engineering Geobacter pili to produce metal:organic filaments. Biosensors and Bioelectronics 2023, 222 , 114993. https://doi.org/10.1016/j.bios.2022.114993
- Jianmei Luo, Wanjun Tian, Hongchen Jin, Jianing Yang, Jinghan Li, Yu Wang, Wenqi Shen, Yaya Ren, Minghua Zhou. Recent advances in microbial fuel cells: A review on the identification technology, molecular tool and improvement strategy of electricigens. Current Opinion in Electrochemistry 2023, 37 , 101187. https://doi.org/10.1016/j.coelec.2022.101187
- Jun Yao, , , , . Protein nanowire thin films for the potential of constructing green electronic devices. 2023, 26. https://doi.org/10.1117/12.2647424
- Daniel Mark Shapiro, Gunasheil Mandava, Sibel Ebru Yalcin, Pol Arranz-Gibert, Peter J. Dahl, Catharine Shipps, Yangqi Gu, Vishok Srikanth, Aldo I. Salazar-Morales, J. Patrick O’Brien, Koen Vanderschuren, Dennis Vu, Victor S. Batista, Nikhil S. Malvankar, Farren J. Isaacs. Protein nanowires with tunable functionality and programmable self-assembly using sequence-controlled synthesis. Nature Communications 2022, 13 (1) https://doi.org/10.1038/s41467-022-28206-x
- Xiaomeng Liu, Toshiyuki Ueki, Hongyan Gao, Trevor L. Woodard, Kelly P. Nevin, Tianda Fu, Shuai Fu, Lu Sun, Derek R. Lovley, Jun Yao. Microbial biofilms for electricity generation from water evaporation and power to wearables. Nature Communications 2022, 13 (1) https://doi.org/10.1038/s41467-022-32105-6
- Fangyuan Dong, Olja Simoska, Erin Gaffney, Shelley D. Minteer. Applying synthetic biology strategies to bioelectrochemical systems. Electrochemical Science Advances 2022, 2 (6) https://doi.org/10.1002/elsa.202100197
- Benjamin Myers, Phil Hill, Frankie Rawson, Katalin Kovács. Enhancing Microbial Electron Transfer Through Synthetic Biology and Biohybrid Approaches: Part II : Combining approaches for clean energy. Johnson Matthey Technology Review 2022, 66 (4) , 455-465. https://doi.org/10.1595/205651322X16621070592195
- Roshni R. Kharadi, Kayla Selbmann, George W. Sundin, . A complete twelve-gene deletion null mutant reveals that cyclic di-GMP is a global regulator of phase-transition and host colonization in Erwinia amylovora. PLOS Pathogens 2022, 18 (8) , e1010737. https://doi.org/10.1371/journal.ppat.1010737
- Zhong Li, Xinyu Wang, Jie Wang, Xinyi Yuan, Xiaoyu Jiang, Yanyi Wang, Chao Zhong, Dake Xu, Tingyue Gu, Fuhui Wang. Bacterial biofilms as platforms engineered for diverse applications. Biotechnology Advances 2022, 57 , 107932. https://doi.org/10.1016/j.biotechadv.2022.107932
- Derek R. Lovley. On the Existence of Pilin-Based Microbial Nanowires. Frontiers in Microbiology 2022, 13 https://doi.org/10.3389/fmicb.2022.872610
- Zhen Fang, Yinjie J Tang, Mattheos AG Koffas. Harnessing electrical-to-biochemical conversion for microbial synthesis. Current Opinion in Biotechnology 2022, 75 , 102687. https://doi.org/10.1016/j.copbio.2022.102687
- Kai Jin, Chenyang Jin, Yihan Wu. Synthetic biology-powered microbial co-culture strategy and application of bacterial cellulose-based composite materials. Carbohydrate Polymers 2022, 283 , 119171. https://doi.org/10.1016/j.carbpol.2022.119171
- Thomas Andrew Clarke. Plugging into bacterial nanowires: a comparison of model electrogenic organisms. Current Opinion in Microbiology 2022, 66 , 56-62. https://doi.org/10.1016/j.mib.2021.12.003
- Derek R. Lovley, Dawn E. Holmes. Electromicrobiology: the ecophysiology of phylogenetically diverse electroactive microorganisms. Nature Reviews Microbiology 2022, 20 (1) , 5-19. https://doi.org/10.1038/s41579-021-00597-6
- Rahul Kandpal, Mohammad Shahadat, S. Wazed Ali, Shaikh Ziauddin Ahammad. Recent technologies for modern and future industry. 2022, 1-20. https://doi.org/10.1016/B978-0-12-823296-5.00004-6
- Lina J. Bird, Fernanda Jiménez Otero, Matthew D. Yates, Brian J. Eddie, Leonard M. Tender, Sarah M. Glaven. Engineered Living Conductive Biofilms. 2022, 95-128. https://doi.org/10.1007/978-3-030-92949-7_4
- Vali Alizadeh. Preparation a novel 1-pyreneacetic acid functionalized graphene/self-assembled monolayer modified gold electrode to immobilize and study interfacial electron transfer of cytochrome c by electrochemical approaches. Chemical Physics Letters 2022, 787 , 139187. https://doi.org/10.1016/j.cplett.2021.139187
- Juntao Zhao, Feng Li, Yingxiu Cao, Xinbo Zhang, Tao Chen, Hao Song, Zhiwen Wang. Microbial extracellular electron transfer and strategies for engineering electroactive microorganisms. Biotechnology Advances 2021, 53 , 107682. https://doi.org/10.1016/j.biotechadv.2020.107682
- Toshiyuki Ueki, David J. F. Walker, Kelly P. Nevin, Joy E. Ward, Trevor L. Woodard, Stephen S. Nonnenmann, Derek R. Lovley, . Generation of High Current Densities in Geobacter sulfurreducens Lacking the Putative Gene for the PilB Pilus Assembly Motor. Microbiology Spectrum 2021, 9 (2) https://doi.org/10.1128/Spectrum.00877-21
- Zhen Fang, Jun Zhou, Xiangtong Zhou, Mattheos A.G. Koffas. Abiotic-biotic hybrid for CO2 biomethanation: From electrochemical to photochemical process. Science of The Total Environment 2021, 791 , 148288. https://doi.org/10.1016/j.scitotenv.2021.148288
- Parini Surti, Suresh Kumar Kailasa, Arvind Kumar Mungray. Genetic engineering strategies for performance enhancement of bioelectrochemical systems: A review. Sustainable Energy Technologies and Assessments 2021, 47 , 101332. https://doi.org/10.1016/j.seta.2021.101332
- Xinying Liu, David J. F. Walker, Stephen S. Nonnenmann, Dezhi Sun, Derek R. Lovley, . Direct Observation of Electrically Conductive Pili Emanating from Geobacter sulfurreducens. mBio 2021, 12 (4) https://doi.org/10.1128/mBio.02209-21
- Toshiyuki Ueki, . Cytochromes in Extracellular Electron Transfer in Geobacter. Applied and Environmental Microbiology 2021, 87 (10) https://doi.org/10.1128/AEM.03109-20
- Olja Simoska, Zayn Rhodes, Samali Weliwatte, Jaime R. Cabrera‐Pardo, Erin M. Gaffney, Koun Lim, Shelley D. Minteer. Advances in Electrochemical Modification Strategies of 5‐Hydroxymethylfurfural. ChemSusChem 2021, 14 (7) , 1674-1686. https://doi.org/10.1002/cssc.202100139
- Dibyojyoty Nath, Indrajit Chakraborty, M.M. Ghangrekar. Integrating microbial electrochemical technologies for methane-to-bioelectricity and water-splitting to impart self-sustainability to wastewater treatment plants. Bioresource Technology Reports 2021, 13 , 100644. https://doi.org/10.1016/j.biteb.2021.100644
- Hyun-Jin Kang, Sang-Hoon Lee, Tae-Guen Lim, Jeong-Hoon Park, Boram Kim, Pierre Buffière, Hee-Deung Park. Recent advances in methanogenesis through direct interspecies electron transfer via conductive materials: A molecular microbiological perspective. Bioresource Technology 2021, 322 , 124587. https://doi.org/10.1016/j.biortech.2020.124587
- Catharine Shipps, H. Ray Kelly, Peter J. Dahl, Sophia M. Yi, Dennis Vu, David Boyer, Calina Glynn, Michael R. Sawaya, David Eisenberg, Victor S. Batista, Nikhil S. Malvankar. Intrinsic electronic conductivity of individual atomically resolved amyloid crystals reveals micrometer-long hole hopping via tyrosines. Proceedings of the National Academy of Sciences 2021, 118 (2) https://doi.org/10.1073/pnas.2014139118
- G. Grasso, D. Zane, R. Dragone. Precision Microbial Nanobiosynthesis: Knowledge, Issues, and Potentiality for the In Vivo Tuning of Microbial Nanomaterials. 2021, 75-112. https://doi.org/10.1007/978-981-33-4777-9_3
- Derek R. Lovley, Jun Yao. Intrinsically Conductive Microbial Nanowires for ‘Green’ Electronics with Novel Functions. Trends in Biotechnology 2021, 43 https://doi.org/10.1016/j.tibtech.2020.12.005
- Sibel Ebru Yalcin, Nikhil S. Malvankar. The blind men and the filament: Understanding structures and functions of microbial nanowires. Current Opinion in Chemical Biology 2020, 59 , 193-201. https://doi.org/10.1016/j.cbpa.2020.08.004
- Morgen M Clark, Gemma Reguera. Biology and biotechnology of microbial pilus nanowires. Journal of Industrial Microbiology and Biotechnology 2020, 47 (9-10) , 897-907. https://doi.org/10.1007/s10295-020-02312-5
- Sophia Roy, Oliver Xie, Noémie‐Manuelle Dorval Courchesne. Challenges in engineering conductive protein fibres: Disentangling the knowledge. The Canadian Journal of Chemical Engineering 2020, 98 (10) , 2081-2095. https://doi.org/10.1002/cjce.23836
- Derek R. Lovley, Dawn E. Holmes, . Protein Nanowires: the Electrification of the Microbial World and Maybe Our Own. Journal of Bacteriology 2020, 202 (20) https://doi.org/10.1128/JB.00331-20
- Xiaomeng Liu, Tianda Fu, Joy Ward, Hongyan Gao, Bing Yin, Trevor Woodard, Derek R. Lovley, Jun Yao. Multifunctional Protein Nanowire Humidity Sensors for Green Wearable Electronics. Advanced Electronic Materials 2020, 6 (9) https://doi.org/10.1002/aelm.202000721
- Alexander F. Smith, Xiaomeng Liu, Trevor L. Woodard, Tianda Fu, Todd Emrick, Juan M. Jiménez, Derek R. Lovley, Jun Yao. Bioelectronic protein nanowire sensors for ammonia detection. Nano Research 2020, 13 (5) , 1479-1484. https://doi.org/10.1007/s12274-020-2825-6