Conductive proteins-based extracellular electron transfer of electroactive microorganisms

Junqi Zhang , Zixuan You , Dingyuan Liu , Rui Tang , Chao Zhao , Yingxiu Cao , Feng Li , Hao Song

Quant. Biol. ›› 2023, Vol. 11 ›› Issue (4) : 405 -420.

PDF (1395KB)
Quant. Biol. ›› 2023, Vol. 11 ›› Issue (4) :405 -420. DOI: 10.1002/qub2.24
REVIEW ARTICLE

Conductive proteins-based extracellular electron transfer of electroactive microorganisms

Author information +
History +
PDF (1395KB)

Abstract

Electroactive microorganisms (EAMs) could utilize extracellular electron transfer (EET) pathways to exchange electrons and energy with their external surroundings. Conductive cytochrome proteins and nanowires play crucial roles in controlling electron transfer rate from cytosol to extracellular electrode. Many previous studies elucidated how the c-type cytochrome proteins and conductive nanowires are synthesized, assembled, and engineered to manipulate the EET rate, and quantified the kinetic processes of electron generation and EET. Here, we firstly overview the electron transfer pathways of EAMs and quantify the kinetic parameters that dictating intracellular electron production and EET. Secondly, we systematically review the structure, conductivity mechanisms, and engineering strategies to manipulate conductive cytochromes and nanowire in EAMs. Lastly, we outlook potential directions for future research in cytochromes and conductive nanowires for enhanced electron transfer. This article reviews the quantitative kinetics of intracellular electron production and EET, and the contribution of engineered c-type cytochromes and conductive nanowire in enhancing the EET rate, which lay the foundation for enhancing electron transfer capacity of EAMs.

Keywords

c-type cytochromes / conductive nanowires / extracellular electron transfer / kinetic parameters / synthetic biology

Cite this article

Download citation ▾
Junqi Zhang, Zixuan You, Dingyuan Liu, Rui Tang, Chao Zhao, Yingxiu Cao, Feng Li, Hao Song. Conductive proteins-based extracellular electron transfer of electroactive microorganisms. Quant. Biol., 2023, 11(4): 405-420 DOI:10.1002/qub2.24

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Yalcin SE, O’Brien JP, Gu Y, Reiss K, Yi SM, Jain R, et al. Electric field stimulates production of highly conductive microbial OmcZ nanowires. Nat Chem Biol. 2020;16:1136–42.

[2]

Zhao J, Li F, Cao Y, Zhang X, Chen T, Song H, et al. Microbial extracellular electron transfer and strategies for engineering electroactive microorganisms. Biotechnol Adv. 2020;53:107682.

[3]

Liu Z, Wang K, Chen Y, Tan T, Nielsen J. Third-generation biorefineries as the means to produce fuels and chemicals from CO2. Nat Catal. 2020;3:274–88.

[4]

Logan BE, Rossi R, Ragab Aa, Saikaly PE. Electroactive microorganisms in bioelectrochemical systems. Nat Rev Microbiol. 2019;17(5):307–19.

[5]

Atkinson JT, Su L, Zhang X, Bennett GN, Silberg JJ, Ajo-Franklin CM. Real-time bioelectronic sensing of environmental contaminants. Nature. 2022;611(7936):548–53.

[6]

Choi S. Electrogenic bacteria promise new opportunities for powering, sensing, and synthesizing. Small. 2022;18:2107902.

[7]

Lu L, Guest JS, Peters CA, Zhu X, Rau GH, Ren ZJ. Waste-water treatment for carbon capture and utilization. Nat Sustain. 2018;1(12):750–8.

[8]

Yu YY, Wang YZ, Fang Z, Shi YT, Cheng QW, Chen YX, et al. Single cell electron collectors for highly efficient wiring-up electronic abiotic/biotic interfaces. Nat Commun. 2020;11(1):4087.

[9]

Ueki T, Walker DJF, Woodard TL, Nevin KP, Nonnenmann SS, Lovley DR. An Escherichia coli chassis for production of electrically conductive protein nanowires. ACS Synth Biol. 2020;9(3):647–54.

[10]

Ueki T, Walker DJF, Tremblay P-L, Nevin KP, Ward JE, Woodard TL, et al. Decorating the outer surface of microbially produced protein nanowires with peptides. ACS Synth Biol. 2019;8:1809–17.

[11]

Su L, Fukushima T, Prior A, Baruch M, Zajdel TJ, Ajo-Franklin CM. Modifying cytochrome c maturation can increase the bioelectronic performance of engineered Escherichia coli. ACS Synth Biol. 2020;9(1):115–24.

[12]

Chabert V, Babel L, Füeg MP, Karamash M, Madivoli ES, Herault N, et al. Kinetics and mechanism of mineral respiration: how iron hemes synchronize electron transfer rates. Angew Chem Int Ed. 2020;59(30):12331–6.

[13]

Ding Q, Liu Q, Zhang Y, Li F, Song H. Modular engineering strategy to redirect electron flux into the electron-transfer chain for enhancing extracellular electron transfer in Shewanella oneidensis. ACS Synth Biol. 2023;12(2):471–81.

[14]

Bonanni PS, Schrott GD, Robuschi L, Busalmen JP. Charge accumulation and electron transfer kinetics in Geobacter sulfurreducens biofilms. Energy Environ Sci. 2012;5(3):6188–95.

[15]

Sanders C, Turkarslan S, Lee D-W, Daldal F. Cytochrome c biogenesis: the Ccm system. Trends Microbiol. 2010;18(6): 266–74.

[16]

Ueki T. Cytochromes in extracellular electron transfer in Geobacter. Appl Environ Microbiol. 2021;87(10):e03109–20.

[17]

Giese B, Karamash M, Fromm KM. Chances and challenges of long-distance electron transfer for cellular redox reactions. FEBS Lett. 2023;597(1):166–73.

[18]

Filman DJ, Marino SF, Ward JE, Yang L, Mester Z, Bullitt E, et al. Cryo-EM reveals the structural basis of long-range electron transport in a cytochrome-based bacterial nanowire. Commun Biol. 2019;2(1):219.

[19]

Desmond-Le Quéméner E, Moscoviz R, Bernet N, Marcus A. Modeling of interspecies electron transfer in anaerobic microbial communities. Curr Opin Biotechnol. 2021;67:49–57.

[20]

Torres CI, Marcus AK, Lee HS, Parameswaran P, Krajmalnik-Brown R, Rittmann BE. A kinetic perspective on extracellular electron transfer by anode-respiring bacteria. FEMS Microbiol Rev. 2010;34(1):3–17.

[21]

Torres CI, Marcus AK, Parameswaran P, Rittmann BE. Kinetic experiments for evaluating the Nernst–Monod model for anode-respiring bacteria (ARB) in a biofilm anode. Environ Sci Technol. 2008;42(17):6593–7.

[22]

Kato Marcus A, Torres CI, Rittmann BE. Conduction-based modeling of the biofilm anode of a microbial fuel cell. Biotechnol Bioeng. 2007;98(6):1171–82.

[23]

Hamelers HVM, ter Heijne A, Stein N, Rozendal RA, Buisman CJN. Butler–Volmer–Monod model for describing bio-anode polarization curves. Bioresour Technol. 2011;102(1):381–7.

[24]

Shi L, Dong H, Reguera G, Beyenal H, Lu A, Liu J, et al. Extracellular electron transfer mechanisms between microorganisms and minerals. Nat Rev Microbiol. 2016;14(10):651–62.

[25]

McMillan DGG, Marritt SJ, Butt JN, Jeuken LJC. Menaquinone-7 is specific cofactor in tetraheme quinol dehydrogenase CymA. J Biol Chem. 2012;287(17):14215–25.

[26]

Beckwith CR, Edwards MJ, Lawes M, Shi L, Butt JN, Richardson DJ, et al. Characterization of MtoD from Sideroxydans lithotrophicus: a cytochrome c electron shuttle used in lithoautotrophic growth. Front Microbiol. 2015;6:00332.

[27]

Marritt SJ, Lowe TG, Bye J, McMillan DGG, Shi L, Fredrickson J, et al. A functional description of CymA, an electron-transfer hub supporting anaerobic respiratory flexibility in Shewanella. Biochem J. 2012;444(3):465–74.

[28]

Dantas JM, Brausemann A, Einsle O, Salgueiro CA. NMR studies of the interaction between inner membrane-associated and periplasmic cytochromes from Geobacter sulfurreducens. FEBS Lett. 2017;591(12):1657–66.

[29]

Levar Caleb E, Chan Chi H, Mehta-Kolte Misha G, Bond Daniel R. An inner membrane cytochrome required only for reduction of high redox potential extracellular electron acceptors. mBio. 2014;5(6):e02034-02014.

[30]

Zacharoff L, Chan CH, Bond DR. Reduction of low potential electron acceptors requires the CbcL inner membrane cytochrome of Geobacter sulfurreducens. Bioelectrochemistry. 2016;107:7–13.

[31]

Antunes JMA, Silva MA, Salgueiro CA, Morgado L. Electron flow from the inner membrane towards the cell exterior in Geobacter sulfurreducens: biochemical characterization of cytochrome CbcL. Front Microbiol. 2022;13:898015.

[32]

Shi L, Rosso KM, Zachara JM, Fredrickson JK. Mtr extracellular electron-transfer pathways in Fe(III)-reducing or Fe(II)- oxidizing bacteria: a genomic perspective. Biochem Soc Trans. 2012;40(6):1261–7.

[33]

Gao H, Yang ZK, Barua S, Reed SB, Romine MF, Nealson KH, et al. Reduction of nitrate in Shewanella oneidensis depends on atypical NAP and NRF systems with NapB as a preferred electron transport protein from CymA to NapA. ISME J. 2009;3(8):966–76.

[34]

Fonseca BM, Paquete CM, Neto SE, Pacheco I, Soares CM, Louro RO. Mind the gap: cytochrome interactions reveal electron pathways across the periplasm of Shewanella oneidensis MR-1. Biochem J. 2013;449(1):101–8.

[35]

Sturm G, Richter K, Doetsch A, Heide H, Louro RO, Gescher J. A dynamic periplasmic electron transfer network enables respiratory flexibility beyond a thermodynamic regulatory regime. ISME J. 2015;9(8):1802–11.

[36]

Alves MN, Neto SE, Alves AS, Fonseca BM, Carrêlo A, Pacheco I, et al. Characterization of the periplasmic redox network that sustains the versatile anaerobic metabolism of Shewanella oneidensis MR-1. Front Microbiol. 2015;6:00665.

[37]

Mowat CG, Rothery E, Miles CS, McIver L, Doherty MK, Drewette K, et al. Octaheme tetrathionate reductase is a respiratory enzyme with novel heme ligation. Nat Struct Mol Biol. 2004;11(10):1023–4.

[38]

Atkinson SJ, Mowat CG, Reid GA, Chapman SK. An octaheme c-type cytochrome from Shewanella oneidensis can reduce nitrite and hydroxylamine. FEBS Lett. 2007;581(20):3805–8.

[39]

Shirodkar S, Reed S, Romine M, Saffarini D. The octahaem SirA catalyses dissimilatory sulfite reduction in Shewanella oneidensis MR-1. Environ Microbiol. 2011;13(1):108–15.

[40]

Lloyd JR, Leang C, Hodges Myerson AL, Coppi MV, Cuifo S, Methe B, et al. Biochemical and genetic characterization of PpcA, a periplasmic c-type cytochrome in Geobacter sulfurreducens. Biochem J. 2003;369(1):153–61.

[41]

Pokkuluri PR, Londer YY, Duke NE, Long WC, Schiffer M. Family of cytochrome C7-type proteins from Geobacter sulfurreducens: structure of one cytochrome C7 at 1.45 A resolution. Biochemistry. 2004;43(4):849–59.

[42]

Morgado L, Bruix M, Pessanha M, Londer YY, Salgueiro CA. Thermodynamic characterization of a triheme cytochrome family from Geobacter sulfurreducens reveals mechanistic and functional diversity. Biophys J. 2010;99(1):293–301.

[43]

Santos TC, Silva MA, Morgado L, Dantas JM, Salgueiro CA. Diving into the redox properties of Geobacter sulfurreducens cytochromes: a model for extracellular electron transfer. Dalton Trans. 2015;44(20):9335–44.

[44]

Fernandes TM, Folgosa F, Teixeira M, Salgueiro CA, Morgado L. Structural and functional insights of GSU0105, a unique multiheme cytochrome from G. sulfurreducens. Biophys J. 2021;120(23):5395–407.

[45]

Teixeira LR, Fernandes TM, Silva MA, Morgado L, Salgueiro CA. Characterization of a novel cytochrome involved in Geobacter sulfurreducens’ electron harvesting pathways. Chem Eur J. 2022;28(66):e202202333.

[46]

Hartshorne RS, Reardon CL, Ross D, Nuester J, Clarke TA, Gates AJ, et al. Characterization of an electron conduit between bacteria and the extracellular environment. Proc Natl Acad Sci USA. 2009;106(52):22169–74.

[47]

Edwards MJ, White GF, Butt JN, Richardson DJ, Clarke TA. The crystal structure of a biological insulated transmembrane molecular wire. Cell. 2020;181(3):665–73.

[48]

Richardson DJ, Butt JN, Fredrickson JK, Zachara JM, Shi L, Edwards MJ, et al. The ‘porin-cytochrome’ model for microbeto- mineral electron transfer. Mol Microbiol. 2012;85(2):201–12.

[49]

White GF, Shi Z, Shi L, Wang Z, Dohnalkova AC, Marshall MJ, et al. Rapid electron exchange between surface-exposed bacterial cytochromes and Fe(III) minerals. Proc Natl Acad Sci USA. 2013;110(16):6346–51.

[50]

Gralnick JA, Vali H, Lies DP, Newman DK. Extracellular respiration of dimethyl sulfoxide by Shewanella oneidensis strain MR-1. Proc Natl Acad Sci USA. 2006;103(12):4669–74.

[51]

Schicklberger M, Sturm G, Gescher J. Genomic plasticity enables a secondary electron transport pathway in Shewanella oneidensis. Appl Environ Microbiol. 2013;79(4):1150–9.

[52]

Liu Y, Wang Z, Liu J, Levar C, Edwards MJ, Babauta JT, et al. A trans-outer membrane porin-cytochrome protein complex for extracellular electron transfer by Geobacter sulfurreducens PCA. Environ Microbiol Rep. 2014;6:776–85.

[53]

Yarzábal A, Brasseur G, Ratouchniak J, Lund K, Lemesle-Meunier D, DeMoss JA, et al. The high-molecular-weight cytochrome c Cyc2 of Acidithiobacillus ferrooxidans is an outer membrane protein. J Bacteriol. 2002;184(1):313–7.

[54]

Jiao Y, Newman DK. The pio operon is essential for phototrophic Fe(II) oxidation in Rhodopseudomonas palustris TIE-1. J Bacteriol. 2007;189(5):1765–73.

[55]

Liu J, Pearce CI, Liu C, Wang Z, Shi L, Arenholz E, et al. Fe(3-x)Ti(x)O4 nanoparticles as tunable probes of microbial metal oxidation. J Am Chem Soc. 2013;135(24):8896–907.

[56]

Bird LJ, Saraiva IH, Park S, Calçada EO, Salgueiro CA, Nitschke W, et al. Nonredundant roles for cytochrome C2 and two high-potential iron-sulfur proteins in the photoferrotroph Rhodopseudomonas palustris TIE-1. J Bacteriol. 2014;196(4):850–8.

[57]

Bose A, Gardel EJ, Vidoudez C, Parra EA, Girguis PR. Electron uptake by iron-oxidizing phototrophic bacteria. Nat Commun. 2014;5(1):3391.

[58]

Shi L, Fredrickson JK, Zachara JM. Genomic analyses of bacterial porin-cytochrome gene clusters. Front Microbiol. 2014;5:657.

[59]

Chan CH, Levar CE, Jiménez-Otero F, Bond DR. Genome scale mutational analysis of Geobacter sulfurreducens reveals distinct molecular mechanisms for respiration and sensing of poised electrodes versus Fe(III) oxides. J Bacteriol. 2017;199(19):e00340-00317.

[60]

Ross DE, Brantley SL, Tien M. Kinetic characterization ofOmcA and MtrC, terminal reductases involved in respiratory electron transfer for dissimilatory iron reduction in Shewanella oneidensis MR-1. Appl Environ Microbiol. 2009;75(16):5218–26.

[61]

Kim BC, Leang C, Ding YH, Glaven RH, Coppi MV, Lovley DR. OmcF, a putative c-type monoheme outer membrane cytochrome required for the expression of other outer membrane cytochromes in Geobacter sulfurreducens. J Bacteriol. 2005;187(13):4505–13.

[62]

Mehta T, Coppi MV, Childers SE, Lovley DR. Outer membrane c-type cytochromes required for Fe(III) and Mn(IV) oxide reduction in Geobacter sulfurreducens. Appl Environ Microbiol. 2005;71(12):8634–41.

[63]

Holmes DE, Chaudhuri SK, Nevin KP, Mehta T, Methé BA, Liu A, et al. Microarray and genetic analysis of electron transfer to electrodes in Geobacter sulfurreducens. Environ Microbiol. 2006;8(10):1805–15.

[64]

Inoue K, Leang C, Franks AE, Woodard TL, Nevin KP, Lovley DR. Specific localization of the c-type cytochrome OmcZ at the anode surface in current-producing biofilms of Geobacter sulfurreducens. Environ Microbiol Rep. 2011;3(2):211–7.

[65]

Zacharoff LA, Morrone DJ, Bond DR. Geobacter sulfurreducens extracellular multiheme cytochrome PgcA facilitates respiration to Fe(iii) oxides but not electrodes. Front Microbiol. 2017;8:2481.

[66]

Carlson HK, Iavarone AT, Gorur A, Yeo BS, Tran R, Melnyk RA, et al. Surface multiheme c-type cytochromes from Thermincola potens and implications for respiratory metal reduction by Gram-positive bacteria. Proc Natl Acad Sci USA. 2012;109(5):1702–7.

[67]

Butler KT, Davies DW, Cartwright H, Isayev O, Walsh A. Machine learning for molecular and materials science. Nature. 2018;559(7715):547–55.

[68]

Jumper J, Evans R, Pritzel A, Green T, Figurnov M, Ronneberger O, et al. Highly accurate protein structure prediction with AlphaFold. Nature. 2021;596(7873):583–9.

[69]

Salgueiro CA, Morgado L, Silva MA, Ferreira MR, Fernandes TM, Portela PC. From iron to bacterial electroconductive filaments: exploring cytochrome diversity using Geobacter bacteria. Coord Chem Rev. 2022;452:214284.

[70]

Paquete CM, Saraiva IH, Louro RO. Redox tuning of the catalytic activity of soluble fumarate reductases from Shewanella. Biochim Biophys Acta Bioenerg. 2014;1837(6):717–25.

[71]

Firer-Sherwood MA, Ando N, Drennan CL, Elliott SJ. Solution-based structural analysis of the decaheme cytochrome, MtrA, by SMALL-ANGLE X-ray scattering and analytical ultracentrifugation. J Phys Chem B. 2011;115(38):11208–14.

[72]

Fernandes TM, Morgado L, Turner DL, Salgueiro CA. Protein engineering of electron transfer components from electroactive Geobacter bacteria. Antioxidants. 2021;10(6):844.

[73]

Simon J, van Spanning RJM, Richardson DJ. The organisation of proton motive and non-proton motive redox loops in prokaryotic respiratory systems. Biochim Biophys Acta Bioenerg. 2008;1777(12):1480–90.

[74]

Vellingiri A, Song YE, Munussami G, Kim C, Park C, Jeon B-H, et al. Overexpression of c-type cytochrome, CymA in Shewanella oneidensis MR-1 for enhanced bioelectricity generation and cell growth in a microbial fuel cell. J Chem Technol Biotechnol. 2019;94(7):2115–22.

[75]

Sun W, Lin Z, Yu Q, Cheng S, Gao H. Promoting extracellular electron transfer of Shewanella oneidensis MR-1 by optimizing the periplasmic cytochrome c network. Front Microbiol. 2021;12:727709.

[76]

Li F, Tang R, Zhang B, Qiao C, Yu H, Liu Q, et al. Systematic full-cycle engineering microbial biofilms to boost electricity production in Shewanella oneidensis. Research. 2023;6:0081.

[77]

Jensen HM, TerAvest MA, Kokish MG, Ajo-Franklin CM. CymA and exogenous flavins improve extracellular electron transfer and couple it to cell growth in Mtr-expressing Escherichia coli. ACS Synth Biol. 2016;5(7):679–88.

[78]

Meyer TE, Tsapin AI, Vandenberghe I, De Smet L, Frishman D, Nealson KH, et al. Identification of 42 possible cytochrome c genes in the Shewanella oneidensis genome and characterization of six soluble cytochromes. OMICS A J Integr Biol. 2004;8(1):57–77.

[79]

Delgado VP, Paquete CM, Sturm G, Gescher J. Improvement of the electron transfer rate in Shewanella oneidensis MR-1 using a tailored periplasmic protein composition. Bioelectrochemistry. 2019;129:18–25.

[80]

Jensen HM, Albers AE, Malley KR, Londer YY, Cohen BE, Helms BA, et al. Engineering of a synthetic electron conduit in living cells. Proc Natl Acad Sci USA. 2010;107(45): 19213–8.

[81]

TerAvest MA, Zajdel TJ, Ajo-Franklin CM. The Mtr pathway of Shewanella oneidensis MR-1 couples substrate utilization to current production in Escherichia coli. Chemelectrochem. 2014;1(11):1874–9.

[82]

Jing X, Wu Y, Shi L, Peacock Caroline L, Ashry Noha M, Gao C, et al. Outer membrane c-type cytochromes OmcA and MtrC play distinct roles in enhancing the attachment of Shewanella oneidensis MR-1 cells to goethite. Appl Environ Microbiol. 2020;86(23):e01941-01920.

[83]

Sekar N, Jain R, Yan Y, Ramasamy RP. Enhanced photobioelectrochemical energy conversion by genetically engineered cyanobacteria. Biotechnol Bioeng. 2016;113(3):675–9.

[84]

Reguera G, McCarthy KD, Mehta T, Nicoll JS, Tuominen MT, Lovley DR. Extracellular electron transfer via microbial nanowires. Nature. 2005;435(7045):1098–101.

[85]

Walker DJ, Adhikari RY, Holmes DE, Ward JE, Woodard TL, Nevin KP, et al. Electrically conductive pili from pilin genes of phylogenetically diverse microorganisms. ISME J. 2018;12(1):48–58.

[86]

Lovley DR, Malvankar NS. Seeing is believing: novel imaging techniques help clarify microbial nanowire structure and function. Environ Microbiol. 2015;17(7):2209–15.

[87]

Gorby YA, Yanina S, McLean JS, Rosso KM, Moyles D, Dohnalkova A, et al. Electrically conductive bacterial nanowires produced by Shewanella oneidensis strain MR-1 and other microorganisms. Proc Natl Acad Sci USA. 2006;103(30): 11358–63.

[88]

Bhaya D, Bianco NR, Bryant D, Grossman A. Type IV pilus biogenesis and motility in the cyanobacterium Synechocystis sp. PCC6803. Mol Microbiol. 2000;37(4):941–51.

[89]

Yang Y, Wang Z, Gan C, Klausen LH, Bonne R, Kong G, et al. Long-distance electron transfer in a filamentous Grampositive bacterium. Nat Commun. 2021;12(1):1709.

[90]

Lovley DR, Holmes DE. Protein nanowires: the electrification of the microbial world and maybe our own. J Bacteriol. 2020;202(20):e00331-00320.

[91]

Holmes DE, Dang Y, Walker DJF, Lovley DR. The electrically conductive pili of Geobacter species are a recently evolved feature for extracellular electron transfer. Microb Genom. 2016;2(8):e000072.

[92]

Bray MS, Wu J, Padilla CC, Stewart FJ, Fowle DA, Henny C, et al. Phylogenetic and structural diversity of aromatically dense pili from environmental metagenomes. Environ Microbiol Rep. 2020;12(1):49–57.

[93]

Lovley DR, Walker DJF. Geobacter protein nanowires. Front Microbiol. 2019;10:2078.

[94]

Lovley DR. Happy together: microbial communities that hook up to swap electrons. ISME J. 2017;11(2):327–36.

[95]

Lovley DR. Electrically conductive pili: biological function and potential applications in electronics. Curr Opin Electrochem. 2017;4(1):190–8.

[96]

Gu Y, Srikanth V, Salazar-Morales AI, Jain R, O’Brien JP, Yi SM, et al. Structure of Geobacter pili reveals secretory rather than nanowire behaviour. Nature. 2021;597(7876):430–4.

[97]

Lampa-Pastirk S, Veazey JP, Walsh KA, Feliciano GT, Steidl RJ, Tessmer SH, et al. Thermally activated charge transport in microbial protein nanowires. Sci Rep. 2016;6(1):23517.

[98]

Tan Y, Adhikari RY, Malvankar NS, Ward JE, Woodard TL, Nevin KP, et al. Expressing the Geobacter metallireducens PilA in Geobacter sulfurreducens yields pili with exceptional conductivity. mBio. 2017;8(1):02203–16.

[99]

Wang F, Coureuil M, Osinski T, Orlova A, Altindal T, Gesbert G, et al. Cryoelectron microscopy reconstructions of the Pseudomonas aeruginosa and Neisseria gonorrhoeae type IV pili at sub-nanometer resolution. Structure. 2017;25(9):1423–35.e1424.

[100]

Walker DJF, Nevin KP, Holmes DE, Rotaru AE, Ward JE, Woodard TL, et al. Syntrophus conductive pili demonstrate that common hydrogen-donating syntrophs can have a direct electron transfer option. ISME J. 2020;14(3):837–46.

[101]

Poweleit N, Ge P, Nguyen HH, Loo RR, Gunsalus RP, Zhou ZH. CryoEM structure of the Methanospirillum hungatei archaellum reveals structural features distinct from the bacterial flagellum and type IV pilus. Nat Microbiol. 2016;2(3):16222.

[102]

Wang F, Gu Y, O’Brien JP, Yi SM, Yalcin SE, Srikanth V, et al. Structure of microbial nanowires reveals stacked hemes that transport electrons over micrometers. Cell. 2019;177:361–9. e310.

[103]

Gu Y, Guberman-Pfeffer MJ, Srikanth V, Shen C, Giska F, Gupta K, et al. Structure of Geobacter cytochrome OmcZ identifies mechanism of nanowire assembly and conductivity. Nat Microbiol. 2023;8(2):284–98.

[104]

Wang F, Mustafa K, Suciu V, Joshi K, Chan CH, Choi S, et al. Cryo-EM structure of an extracellular Geobacter OmcE cytochrome filament reveals tetrahaem packing. Nat Microbiol. 2022;7(8):1291–300.

[105]

Malvankar NS, Vargas M, Nevin K, Tremblay PL, Evans-Lutterodt K, Nykypanchuk D, et al. Structural basis for metallic-like conductivity in microbial nanowires. mBio. 2015;6(2):e00084.

[106]

Steidl RJ, Lampa-Pastirk S, Reguera G. Mechanistic stratification in electroactive biofilms of Geobacter sulfurreducens mediated by pilus nanowires. Nat Commun. 2016;7(1):12217.

[107]

Adhikari RY, Malvankar NS, Tuominen MT, Lovley DR. Conductivity of individual Geobacter pili. RSC Adv. 2016;6(10): 8354–7.

[108]

Vargas M, Malvankar NS, Tremblay PL, Leang C, Smith JA, Patel P, et al. Aromatic amino acids required for pili conductivity and long-range extracellular electron transport in Geobacter sulfurreducens. mBio. 2013;4(2):e00105–13.

[109]

Tan Y, Adhikari RY, Malvankar NS, Pi S, Ward JE, Woodard TL, et al. Synthetic biological protein nanowires with high conductivity. Small. 2016;12(33):4481–5.

[110]

Tan Y, Adhikari RY, Malvankar NS, Ward JE, Nevin KP, Woodard TL, et al. The low conductivity of Geobacter uraniireducens pili suggests a diversity of extracellular electron transfer mechanisms in the genus Geobacter. Front Microbiol. 2016;7:980.

[111]

Liu X, Tremblay PL, Malvankar NS, Nevin KP, Lovley DR, Vargas M. A Geobacter sulfurreducens strain expressing Pseudomonas aeruginosa type IV pili localizes OmcS on pili but is deficient in Fe(III) oxide reduction and current production. Appl Environ Microbiol. 2014;80(3):1219–24.

[112]

Malvankar NS, Vargas M, Nevin KP, Franks AE, Leang C, Kim BC, et al. Tunable metallic-like conductivity in microbial nanowire networks. Nat Nanotechnol. 2011;6(9):573–9.

[113]

Long Y-Z, Li M-M, Gu C, Wan M, Duvail J-L, Liu Z, et al. Recent advances in synthesis, physical properties and applications of conducting polymer nanotubes and nanofibers. Prog Polym Sci. 2011;36(10):1415–42.

[114]

Malvankar NS, Lovley DR. Microbial nanowires: a new paradigm for biological electron transfer and bioelectronics. ChemSusChem. 2012;5(6):1039–46.

[115]

Giese B. Electron transfer through DNA and peptides. Bioorg Med Chem. 2006;14(18):6139–43.

[116]

Martinez CR, Iverson BL. Rethinking the term “pi-stacking”. Chem Sci. 2012;3(7):2191.

[117]

Himmelberger S, Salleo A. Engineering semiconducting polymers for efficient charge transport. MRS Commun. 2015;5(3):383–95.

[118]

Yan H, Chuang C, Zhugayevych A, Tretiak S, Dahlquist FW, Bazan GC. Inter-aromatic distances in Geobacter sulfurreducens pili relevant to biofilm charge transport. Adv Mater. 2015;27(11):1908–11.

[119]

Lebedev N, Mahmud S, Griva I, Blom A, Tender LM. On the electron transfer through Geobacter sulfurreducens PilA protein. J Polym Sci B Polym Phys. 2015;53(24):1706–17.

[120]

Waleed Shinwari M, Jamal Deen M, Starikov EB, Cuniberti G. Electrical conductance in biological molecules. Adv Funct Mater. 2010;20(12):1865–83.

[121]

Lovley DR, Yao J. Intrinsically conductive microbial nanowires for ‘green’ electronics with novel functions. Trends Biotechnol. 2021;39(9):940–52.

[122]

Liu X, Wang S, Xu A, Zhang L, Liu H, Ma LZ. Biological synthesis of high-conductive pili in aerobic bacterium Pseudomonas aeruginosa. Appl Microbiol Biotechnol. 2019;103(3): 1535–44.

[123]

Shapiro DM, Mandava G, Yalcin SE, Arranz-Gibert P, Dahl PJ, Shipps C, et al. Protein nanowires with tunable functionality and programmable self-assembly using sequence-controlled synthesis. Nat Commun. 2022;13(1):829.

[124]

Liu X, Gao H, Ward JE, Liu X, Yin B, Fu T, et al. Power generation from ambient humidity using protein nanowires. Nature. 2020;578(7796):550–4.

[125]

Ahmad R, Mahmoudi T, Ahn MS, Hahn YB. Recent advances in nanowires-based field-effect transistors for biological sensor applications. Biosens Bioelectron. 2018;100:312–25.

[126]

Tran DP, Pham TTT, Wolfrum B, Offenhausser A, Thierry B. CMOS-compatible silicon nanowire field-effect transistor biosensor: technology development toward commercialization. Materials. 2018;11(5):785.

[127]

Ing NL, Nusca TD, Hochbaum AI. Geobacter sulfurreducens pili support ohmic electronic conduction in aqueous solution. Phys Chem Chem Phys. 2017;19(32):21791–9.

[128]

Yates MD, Strycharz-Glaven SM, Golden JP, Roy J, Tsoi S, Erickson JS, et al. Measuring conductivity of living Geobacter sulfurreducens biofilms. Nat Nanotechnol. 2016;11:910–3.

[129]

Stokes JM, Yang K, Swanson K, Jin W, Cubillos-Ruiz A, Donghia NM, et al. A deep learning approach to antibiotic discovery. Cell. 2020;180(4):688–702.e613.

[130]

Chong GW, Karbelkar AA, El-Naggar MY. Nature’s conductors: what can microbial multi-heme cytochromes teach us about electron transport and biological energy conversion? Curr Opin Chem Biol. 2018;47:7–17.

[131]

Zhang H, Liu H, Tian Z, Lu D, Yu Y, Cestellos-Blanco S, et al. Bacteria photosensitized by intracellular gold nanoclusters for solar fuel production. Nat Nanotechnol. 2018;13(10):900–5.

[132]

Yu W, Bai H, Zeng Y, Zhao H, Xia S, Huang Y, et al. Solar-driven producing of value-added chemicals with organic semiconductor-bacteria biohybrid system. Research. 2022;2022:9834093.

[133]

Sakimoto KK, Wong AB, Yang P. Self-photosensitization of nonphotosynthetic bacteria for solar-to-chemical production. Science. 2016;351(6268):74–7.

[134]

Hu G, Li Z, Ma D, Ye C, Zhang L, Gao C, et al. Light-driven CO2 sequestration in Escherichia coli to achieve theoretical yield of chemicals. Nat Catal. 2021;4(5):395–406.

[135]

Guo J, Suástegui M, Sakimoto KK, Moody VM, Xiao G, Nocera DG, et al. Light-driven fine chemical production in yeast biohybrids. Science. 2018;362(6416):813–6.

[136]

Sahoo PC, Pant D, Kumar M, Puri SK, Ramakumar SSV. Material–microbe interfaces for solar-driven CO2 bioelectrosynthesis. Trends Biotechnol. 2020;38(11):1245–61.

[137]

Su Y, Cestellos-Blanco S, Kim JM, Shen Y-X, Kong Q, Lu D, et al. Close-packed nanowire-bacteria hybrids for efficient solar-driven CO2 fixation. Joule. 2020;4:800–11.

RIGHTS & PERMISSIONS

2023 The Authors. Quantitative Biology published by John Wiley & Sons Australia, Ltd on behalf of Higher Education Press.

AI Summary AI Mindmap
PDF (1395KB)

790

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/