Structural basis for metallic-like conductivity in microbial nanowires

mBio

Volumn 6, Issue 2, 2015, Pages

  Malvankar, Nikhil S ^a   Vargas, Madeline ^a,b   Nevin, Kelly ^a   Tremblay, Pier Luc ^a,d   Evans Lutterodt, Kenneth ^c   Nykypanchuk, Dmytro ^c   Martz, Eric ^a   Tuomine, Mark T ^a   Lovley, Derek R ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

^b Department of Biology   (United States)

^c BROOKHAVEN NATIONAL LABORATORY   (United States)

^d TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC AMINO ACID; MICROBIAL NANOWIRE; NANOWIRE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; BACTERIUM PILUS; CONDUCTANCE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ELECTRON TRANSPORT; GEOBACTER SULFURREDUCENS; NEISSERIA GONORRHOEAE; NONHUMAN; PH; PRIORITY JOURNAL; PROTON TRANSPORT; PSEUDOMONAS AERUGINOSA; X RAY DIFFRACTION; CHEMICAL PHENOMENA; CHEMISTRY; DRUG EFFECTS; ELECTROPHYSIOLOGY; FIMBRIA; GEOBACTER; MOLECULAR MODEL; PHYSIOLOGY;

GEOBACTER SULFURREDUCENS; NEISSERIA GONORRHOEAE; PSEUDOMONAS AERUGINOSA;

AMINO ACIDS, AROMATIC; CHEMICAL PHENOMENA; ELECTROPHYSIOLOGICAL PHENOMENA; FIMBRIAE, BACTERIAL; GEOBACTER; HYDROGEN-ION CONCENTRATION; MODELS, MOLECULAR; NANOWIRES; X-RAY DIFFRACTION;

EID: 84929494201     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00084-15     Document Type: Article

References (51)

1. Malvankar NS, Lovley DR. 2012. Microbial nanowires: a new paradigm for biological electron transfer and bioelectronics. ChemSusChem 5:1039–1046. http://dx.doi.org/10.1002/cssc.201100733.
2. Malvankar NS, Lovley DR. 2014. Microbial nanowires for bioenergy applications. Curr Opin Biotechnol 27:88–95. http://dx.doi.org/10.1016/j.copbio.2013.12.003.
3. Lovley DR, Ueki T, Zhang T, Malvankar NS, Shrestha PM, Flanagan KA, Aklujkar M, Butler JE, Giloteaux L, Rotaru AE, Holmes DE, Franks AE, Orellana R, Risso C, Nevin KP. 2011. Geobacter: the microbe electric’s physiology, ecology, and practical applications. Adv Microb Physiol 59:1–100. http://dx.doi.org/10.1016/B978-0-12-387661-4.00004-5.
4. Lovley DR, Nevin KP. 2013. Electrobiocommodities: powering microbial production of fuels and commodity chemicals from carbon dioxide with electricity. Curr Opin Biotechnol 24:385–390. http://dx.doi.org/10.1016/j.copbio.2013.02.012.
5. Edwards PP, Gray HB, Lodge MTJ, Williams RJP. 2008. Electron transfer and electronic conduction through an intervening medium. Angew Chem Int Ed Engl 47:6758–6765. http://dx.doi.org/10.1002/anie.200703177.
6. Malvankar NS, Vargas M, Nevin KP, Franks AE, Leang C, Kim BC, Inoue K, Mester T, Covalla SF, Johnson JP, Rotello VM, Tuominen MT, Lovley DR. 2011. Tunable metallic-like conductivity in microbial nanowire networks. Nat Nanotechnol 6:573–579. http://dx.doi.org/10.1038/nnano.2011.119.
7. Reguera G, McCarthy KD, Mehta T, Nicoll JS, Tuominen MT, Lovley DR. 2005. Extracellular electron transfer via microbial nanowires. Nature 435:1098–1101. http://dx.doi.org/10.1038/nature03661.
8. Rotaru A, Shrestha PM, Liu F, Shrestha M, Shrestha D, Embree M, Zengler K, Wardman C, Nevin KP, Lovley DR. 2014. A new model for electron flow during anaerobic digestion: direct interspecies electron transfer to Methanosaeta for the reduction of carbon dioxide to methane. Energy Environ Sci 7:408–415. http://dx.doi.org/10.1039/c3ee42189a.
9. Rotaru AE, Shrestha PM, Liu F, Markovaite B, Chen S, Nevin KP, Lovley DR. 2014. Direct interspecies electron transfer between Geobacter metallireducens and Methanosarcina barkeri. Appl Environ Microbiol 80: 4599–4605. http://dx.doi.org/10.1128/AEM.00895-14.
10. Malvankar NS, Tuominen MT, Lovley DR. 2012. Biofilm conductivity is a decisive variable for high-current-density microbial fuel cells. Energy Environ Sci 5:5790–5797. http://dx.doi.org/10.1039/c2ee03388g.
11. Reguera G, Nevin KP, Nicoll JS, Covalla SF, Woodard TL, Lovley DR. 2006. Biofilm and nanowire production leads to increased current in Geobacter sulfurreducens fuel cells. Appl Environ Microbiol 72:7345–7348. http://dx.doi.org/10.1128/AEM.01444-06.
12. Nevin KP, Kim BC, Glaven RH, Johnson JP, Woodard TL, Methé BA, DiDonato RJ, Jr, Covalla SF, Franks AE, Liu A, Lovley DR. 2009. Anode biofilm transcriptomics reveals outer surface components essential for high density current production in Geobacter sulfurreducens fuel cells. PLoS One 4:e5628. http://dx.doi.org/10.1371/journal.pone.0005628.
13. Malvankar NS, Yalcin SE, Tuominen MT, Lovley DR. 2014. Visualization of charge propagation along individual pili proteins using ambient electrostatatic force microscopy. Nat Nanotechnol 9:1012–1017. http://dx.doi.org/10.1038/nnano.2014.236.
14. Lovley DR, Malvankar NS. 11 November 2014. Seeing is believing: novel imaging techniques help clarify microbial nanowire structure and function. Environ Microbiol http://dx.doi.org/10.1111/1462-2920.12708.
15. Qian F, Li Y. 2011. Biomaterials: a natural source of nanowires. Nat Nanotechnol 6:538–539. http://dx.doi.org/10.1038/nnano.2011.148.
16. Lee K, Cho S, Park SH, Heeger AJ, Lee CW, Lee SH. 2006. Metallic transport in polyaniline. Nature 441:65-68. http://dx.doi.org/10.1038/nature04705.
17. Vargas M, Malvankar NS, Tremblay PL, Leang C, Smith JA, Patel P, Snoeyenbos-West O, Nevin KP, Lovley DR. 2013. Aromatic amino acids required for pili conductivity and long-range extracellular electron transport in Geobacter sulfurreducens. Mbio 4(2):e00105-13. http://dx.doi.org/10.1128/mBio.00105-13.
18. Liu X, Tremblay P-L, Malvankar NS, Nevin KP, Lovley DR, Vargas M. 2014. 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 80: 1219–1224. http://dx.doi.org/10.1128/AEM.02938-13.
19. Bonanni PS, Massazza D, Busalmen JP. 2013. Stepping stones in the electron transport from cells to electrodes in Geobacter sulfurreducens biofilms. Phys Chem Chem Phys 15:10300-10306. http://dx.doi.org/10.1039/c3cp50411e.
20. Boesen T, Nielsen LP. 2013. Molecular dissection of bacterial nanowires. mBio 4(3):e00270-13. http://dx.doi.org/10.1128/mBio.00270-13.
21. Reardon PN, Mueller KT. 2013. Structure of the type IVa major pilin from the electrically conductive bacterial nanowires of Geobacter sulfurreducens. J Biol Chem 288:29260-29266. http://dx.doi.org/10.1074/jbc.M113.498527.
22. Feliciano GT, Feliciano GT, da Silva AJ, Reguera G, Artacho E. 2012. Molecular and electronic structure of the peptide subunit of Geobacter sulfurreducens conductive pili from first principles. J Phys Chem A 116: 8023–8030. http://dx.doi.org/10.1021/jp302232p.
23. Craig L, Volkmann N, Arvai AS, Pique ME, Yeager M, Egelman EH, Tainer JA. 2006. Type IV pilus structure by cryo-electron microscopy and crystallography: implications for pilus assembly and functions. Mol Cell 23:651–662. http://dx.doi.org/10.1016/j.molcel.2006.07.004.
24. Craig L, Pique ME, Tainer JA. 2004. Type IV pilus structure and bacterial pathogenicity. Nat Rev Microbiol 2:363–378. http://dx.doi.org/10.1038/nrmicro885.
25. Xu H, Das AK, Horie M, Shaik MS, Smith AM, Luo Y, Lu X, Collins R, Liem SY, Song A, Popelier PL, Turner ML, Xiao P, Kinloch IA, Ulijn RV. 2010. An investigation of the conductivity of peptide nanotube networks prepared by enzyme-triggered self-assembly. Nanoscale 2:960–966. http://dx.doi.org/10.1039/b9nr00233b.
26. Martinez CR, Iverson BL. 2012. Rethinking the term “pi-stacking”. Chem Sci 3:2191–2201. http://dx.doi.org/10.1039/c2sc20045g.
27. Janiak C. 2000. A critical account on π-π stacking in metal complexes with aromatic nitrogen-containing ligands. J Chem Soc Dalton Trans 2000:3885–3896. http://dx.doi.org/10.1039/b003010o.
28. Volz HM, Matyi RJ. 1999. High-resolution X-ray diffraction analyses of protein crystals. Philos Trans R Soc Lond A 357:2789-2799. http://dx.doi.org/10.1098/rsta.1999.0466.
29. Lübbert D, Meents A, Weckert E. 2004. Accurate rocking-curve measurements on protein crystals grown in a homogeneous magnetic field of 2.4 T. Acta Crystallogr D Biol Crystallogr 60:987–998. http://dx.doi.org/10.1107/S0907444904005268.
30. Brédas J-L, Beljonne D, Coropceanu V, Cornil J. 2004. Charge-transfer and energy-transfer processes in π-conjugated oligomers and polymers: a molecular picture. Chem Rev 104:4971–5004. http://dx.doi.org/10.1021/cr040084k.
31. Brédas JL, Calbert JP, da Silva Filho DA, Cornil J. 2002. Organic semiconductors: a theoretical characterization of the basic parameters governing charge transport. Proc Natl Acad Sci U S A 99:5804-5809. http://dx.doi.org/10.1073/pnas.092143399.
32. Diegelmann SR, Gorham JM, Tovar JD. 2008. One-dimensional optoelectronic nanostructures derived from the aqueous self-assembly of piconjugated oligopeptides. J Am Chem Soc 130:13840-13841. http://dx.doi.org/10.1021/ja805491d.
33. Vadehra GS, Wall BD, Diegelmann SR, Tovar JD. 2010. On-resin dimerization incorporates a diverse array of π-conjugated functionality within aqueous self-assembling peptide backbones. Chem Commun 46: 3947–3949. http://dx.doi.org/10.1039/c0cc00301h.
34. Malvankar NS, Tuominen MT, Lovley DR. 2012. Lack of cytochrome involvement in long-range electron transport through conductive biofilms and nanowires of Geobacter sulfurreducens. Energy Environ Sci 5:8651–8659. http://dx.doi.org/10.1039/c2ee22330a.
35. Craig L, Taylor RK, Pique ME, Adair BD, Arvai AS, Singh M, Lloyd SJ, Shin DS, Getzoff ED, Yeager M, Forest KT, Tainer JA. 2003. Type IV pilin structure and assembly: X-ray and EM analyses of Vibrio cholerae toxin-coregulated pilus and Pseudomonas aeruginosa PAK pilin. Mol Cell 11:1139–1150. http://dx.doi.org/10.1016/S1097-2765(03)00170-9.
36. Ashkenasy N, Horne WS, Ghadiri MR. 2006. Design of self-assembling peptide nanotubes with delocalized electronic states. Small 2:99-102. http://dx.doi.org/10.1002/smll.200500252.
37. Glaeser RM. 2013. Stroboscopic imaging of macromolecular complexes. Nat Methods 10:475–476. http://dx.doi.org/10.1038/nmeth.2486.
38. Yi H, Nevin KP, Kim BC, Franks AE, Klimes A, Tender LM, Lovley DR. 2009. Selection of a variant of Geobacter sulfurreducens with enhanced capacity for current production in microbial fuel cells. Biosens Bioelectron 24:3498–3503. http://dx.doi.org/10.1016/j.bios.2009.05.004.
39. Smith JA, Tremblay P-L, Shrestha PM, Snoeyenbos-West OL, Franks AE, Nevin KP, Lovley DR. 2014. Going wireless: Fe(III) oxide reduction without pili by Geobacter sulfurreducens strain JS-1. Appl Environ Microbiol 80:4331–4340. http://dx.doi.org/10.1128/AEM.01122-14.
40. Nevin KP, Richter H, Covalla SF, Johnson JP, Woodard TL, Orloff AL, Jia H, Zhang M, Lovley DR. 2008. Power output and coulombic efficiencies from biofilms of Geobacter sulfurreducens comparable to mixed community microbial fuel cells. Environ Microbiol 10:2505–2514.
41. Hélaine S, Carbonnelle E, Prouvensier L, Beretti JL, Nassif X, Pelicic V. 2005. PilX, a pilus-associated protein essential for bacterial aggregation, is a key to pilus-facilitated attachment of Neisseria meningitidis to human cells. Mol Microbiol 55:65–77. http://dx.doi.org/10.1111/j.1365-2958.2004.04372.x.
42. Roine E, Wei W, Yuan J, Nurmiaho-Lassila EL, Kalkkinen N, Romantschuk M, He SY. 1997. Hrp pilus: an hrp-dependent bacterial surface appendage produced by Pseudomonas syringae pv. tomato DC3000. Proc Natl Acad Sci U S A 94:3459-3464. http://dx.doi.org/10.1073/pnas.94.7.3459.
43. Chiang J, MacDiarmid AG. 1986. “Polyaniline”: protonic acid doping of the emeraldine form to the metallic regime. Synth Met 13:193–205. http://dx.doi.org/10.1016/0379-6779(86)90070-6.
44. Cancedda R, Cedola A, Giuliani A, Komlev V, Lagomarsino S, Mastrogiacomo M, Peyrin F, Rustichelli F. 2007. Bulk and interface investigations of scaffolds and tissue-engineered bones by X-ray microtomography and X-ray microdiffraction. Biomaterials 28:2505–2524. http://dx.doi.org/10.1016/j.biomaterials.2007.01.022.
45. Gallaway JW, Gaikwad AM, Hertzberg B, Erdonmez CK, Chen-Wiegart Y-K, Sviridov LA, Evans-Lutterodt K, Wang J, Banerjee S, Steingart DA. 2013. An in situ synchrotron study of zinc anode planarization by a bismuth additive. J Electrochem Soc 161:A275–A284. http://dx.doi.org/10.1149/2.037403jes.
46. Hammersley AP. 1997. FIT2D: an introduction and overview. ESRF, Grenoble, France.
47. Chen VB, Arendall WB, III, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS, Richardson DC. 2010. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 66:12–21. http://dx.doi.org/10.1107/S0907444909042073.
48. Benkert P, Biasini M, Schwede T. 2011. Toward the estimation of the absolute quality of individual protein structure models. Bioinformatics 27:343–350. http://dx.doi.org/10.1093/bioinformatics/btq662.
49. Ashkenazy H, Erez E, Martz E, Pupko T, Ben-Tal N. 2010. ConSurf 2010: calculating evolutionary conservation in sequence and structure of proteins and nucleic acids. Nucleic Acids Res 38:W529–W533. http://dx.doi.org/10.1093/nar/gkq399.
50. Hanson RM. 2010. Jmol—a paradigm shift in crystallographic visualization. J Appl Crystallogr 43:1250-1260. http://dx.doi.org/10.1107/S0021889810030256.
51. Bondi A. 1964. Van der Waals volumes and radii. J Phys Chem 68: 441–451. http://dx.doi.org/10.1021/j100785a001.