Seeing is believing: Novel imaging techniques help clarify microbial nanowire structure and function

Environmental Microbiology

Volumn 17, Issue 7, 2015, Pages 2209-2215

  Lovley, Derek R ^a   Malvankar, Nikhil S ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GEOBACTER SULFURREDUCENS; SHEWANELLA ONEIDENSIS;

CYTOCHROME; FERRIC ION; NANOWIRE; OXIDE;

ATOMIC FORCE MICROSCOPY; ELECTRIC CONDUCTIVITY; ELECTRON; ELECTRON TRANSPORT; FIMBRIA; GEOBACTER; METABOLISM; PERIPLASM; PHYSIOLOGY; SHEWANELLA; ULTRASTRUCTURE;

CYTOCHROMES; ELECTRIC CONDUCTIVITY; ELECTRON TRANSPORT; ELECTRONS; FERRIC COMPOUNDS; FIMBRIAE, BACTERIAL; GEOBACTER; MICROSCOPY, ATOMIC FORCE; NANOWIRES; OXIDES; PERIPLASM; SHEWANELLA;

EID: 84937073803     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12708     Document Type: Article

References (69)

1. Barboza, A., Gomes, A., Archanjo, B., Araujo, P., Jorio, A., Ferlauto, A., etal. (2008) Deformation induced semiconductor-metal transition in single wall carbon nanotubes probed by electric force microscopy. Phys Rev Lett 100: 256804.
2. Berleman, J., and Auer, M. (2013) The role of bacterial outer membrane vesicles for intra-and interspecies delivery. Environ Microbiol 15: 347-354.
3. Boesen, T., and Nielsen, L.P. (2013) Molecular dissection of bacterial nanowires. mBio 4: e00270-13.
4. Bonanni, S., Massazza, D., and Busalmen, J.P. (2013) Stepping stones in the electron transport from cells to electrodes in Geobacter sulfurreducens biofilms. Phys Chem Chem Phys 15: 10300-10306.
5. Brutinel, E., and Gralnick, J. (2012) Shuttling happens: soluble flavin mediators of extracellular electron transfer in Shewanella. Appl Microbiol Biotechnol 93: 41-48.
6. Chen, S., Rotaru, A.-E., Liu, F., Philips, J., Woodard, T., Nevin, K.P., and Lovley, D.R. (2014a) Carbon cloth stimulates direct interspecies electron transfer in syntrophic co-cultures. Bioresour Technol 173: 82-84.
7. Chen, S., Rotaru, A.-E., Shrestha, P.M., Malvankar, N.S., Liu, F., Fan, W., etal. (2014b) Promoting interspecies electron transfer with biochar. Sci Rep 4: 5019.
8. Childers, S.E., Ciufo, S., and Lovley, D.R. (2002) Geobacter metallireducens accesses insoluble Fe(III) oxide by chemotaxis. Nature 416: 767-769.
9. Comolli, L.R., and Banfield, J.F. (2014) Inter-species interconnections in acid mine drainage microbial communities. Front Microbiol 5: 367.
10. Comolli, L.R., Baker, B.J., Downing, K.H., Siegerist, C.E., and Banfield, J.F. (2008) Three-dimensional analysis of the structure and ecology of a novel, ultra-small archaeon. ISME J 3: 159-167.
11. Craig, L., Pique, M.E., and Tainer, J.A. (2004) Type IV pilus structure and bacterial pathogenicity. Nat Rev Microbiol 2: 363-378.
12. Dautel, O.J., Robitzer, M., Flores, J.-C., Tondelier, D., Serein-Spirau, F., Lère-Porte, J.-P., etal. (2008) Electroactive nanorods and nanorings designed by supramolecular association of π-conjugated oligomers. Chem Eur J 14: 4201-4213.
13. Dohnalkova, A.C., Marshall, M.J., Arey, B.W., Williams, K.H., Buck, E.C., and Fredrickson, J.K. (2011) Imaging hydrated microbial extracellular polymers: Comparative analysis by electron microscopy. Appl Environ Microbiol 77: 1254-1262.
14. Dubey, G.P., and Ben-Yehuda, S. (2011) Intercellular nanotubes mediate bacterial communication. Cell 144: 590-600.
15. El-Naggar, M.Y., Gorby, Y.A., Xia, W., and Nealson, K.H. (2008) The molecular density of states in bacterial nanowires. Biophys J 95: 10-12.
16. El-Naggar, M.Y., Wanger, G., Leung, K.M., Yuzvinsky, T.D., Southam, G., Yang, J., etal. (2010) Electrical transport along bacterial nanowires from Shewanella oneidensis MR-1. PNAS 107: 18127-18131.
17. Feliciano, G.T., da Silva, A.J.R., Reguera, G., and 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.
18. Fredrickson, J.K., Romine, M.F., Beliaev, A.S., Auchtung, J.M., Driscoll, M.E., Gardner, T.S., etal. (2008) Towards environmental systems biology of Shewanella. Nat Rev Microbiol 6: 592-603.
19. Giltner, C.L., Nguyen, Y., and Burrows, L.L. (2012) Type IV pilin proteins: versatile molecular modules. Microbiol Mol Biol Rev 76: 740-772.
20. Glaeser, R.M. (2013) Stroboscopic imaging of macromolecular complexes. Nat Methods 10: 475-476.
21. Gorby, Y.A., Yanina, S., McLean, J.S., Rosso, K.M., Moyles, D., Dohnalkova, A., etal. (2006) Electrically conductive bacterial nanowires produced by Shewanella oneidensis strain MR-1 and other microorganisms. PNAS 103: 11358-11363.
22. Hau, H.H., and Gralnick, J.A. (2007) Ecology and biotechnology of the genus Shewanella. Annu Rev Microbiol 61: 237-258.
23. Heeger, A.J. (2001) Semiconducting and metallic polymers: the fourth generation of polymeric materials (Nobel lecture). Angew Chem Int Ed 40: 2591-2611.
24. Heim, T., Lmimouni, K., and Vuillaume, D. (2004) Ambipolar charge injection and transport in a single pentacene monolayer island. Nano Lett 4: 2145-2150.
25. Jahn, U., Gallenberger, M., Junglas, B., Eisenreich, W., Stetter, K.O., Rachel, R., and Huber, H. (2008) Nanoarchaeum equitans and Ignicoccus hospitalis: new insights into a unique, intimate association of two archaea. J Bacteriol 190: 1743-1750.
26. Kashefi, K., and Lovley, D.R. (2003) Extending the upper temperature limit for life. Science 301: 934.
27. Kato, S., Hashimoto, K., and Watanabe, K. (2012) Microbial interspecies electron transfer via electric currents through conductive minerals. PNAS 109: 10042-10046.
28. Leang, C., Qian, X., Mester, T., and Lovley, D.R. (2010) Alignment of the c-type cytochrome OmcS along pili of Geobacter sulfurreducens. Appl Environ Microbiol 76: 4080-4084.
29. Leang, C., Malvankar, N.S., Franks, A.E., Nevin, K.P., and Lovley, D.R. (2013) Engineering Geobacter sulfurreducens to produce a highly cohesive conductive matrix with enhanced capacity for current production. Energy Environ Sci 6: 1901-1908.
30. Leung, K.M., Wanger, G., El-Naggar, M.Y., Gorby, Y., Southam, G., Lau, W.M., and Yang, J. (2013) Shewanella oneidensis MR-1 bacterial nanowires exhibit p-type, tunable electronic behavior. Nano Lett 13: 2407-2411.
31. Liu, F., Rotaru, A.-E., Shrestha, P.M., Malvankar, N.S., Nevin, K.P., and Lovley, D.R. (2012) Promoting direct interspecies electron transfer with activated carbon. Energy Environ Sci 5: 8982-8989.
32. Liu, F., Rotaru, A.-E., Shrestha, P.M., Malvankar, N.S., Nevin, K.P., and Lovley, D.R. (2014a) Magnetite compensates for the lack of a pilin-associated c-type cytochrome in extracellular electron exchange. Environ Microbiol Early View. doi:10.1111/1462-2920.12485.
33. Liu, X., Tremblay, P.-L., Malvankar, N.S., Nevin, K.P., Lovley, D.R., and Vargas, M. (2014b) 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.
34. Lovley, D. (2011a) Reach out and touch someone: potential impact of DIET (direct interspecies energy transfer) on anaerobic biogeochemistry, bioremediation, and bioenergy. Rev Environ Sci Bio/Technol 10: 101-105.
35. Lovley, D.R. (2011b) Live wires: direct extracellular electron exchange for bioenergy and the bioremediation of energy-related contamination. Energy Environ Sci 4: 4896-4906.
36. Lovley, D.R. (2012) Electromicrobiology. Annu Rev Microbiol 66: 391-409.
37. Lovley, D.R., Ueki, T., Zhang, T., Malvankar, N.S., Shrestha, P.M., Flanagan, K., etal. (2011) Geobacter: the microbe electric's physiology, ecology, and practical applications. Adv Microb Physiol 59: 1-100.
38. McCaig, W.D., Koller, A., and Thanassi, D.G. (2013) Production of outer membrane vesicles and outer membrane tubes by Francisella novicida. J Bacteriol 195: 1120-1132.
39. Malvankar, N.S., and Lovley, D.R. (2012) Microbial nanowires: a new paradigm for biological electron transfer and bioelectronics. Chem Sus Chem 5: 1039-1046.
40. Malvankar, N.S., and Lovley, D.R. (2014) Microbial nanowires for bioenergy applications. Curr Opin Biotechnol 27: 88-95.
41. Malvankar, N.S., Vargas, M., Nevin, K.P., Franks, A.E., Leang, C., Kim, B.C., etal. (2011) Tunable metallic-like conductivity in microbial nanowire networks. Nat Nanotechnol 6: 573-579.
42. Malvankar, N.S., Tuominen, M.T., and Lovley, D.R. (2012a) Lack of cytochrome involvement in long-range electron transport through conductive biofilms and nanowires of Geobacter sulfurreducens. Energy Environ Sci 5: 8651-8659.
43. Malvankar, N.S., Tuominen, M.T., and Lovley, D.R. (2012b) Biofilm conductivity is a decisive variable for high-current-density microbial fuel cells. Energy Environ Sci 5: 5790-5797.
44. Malvankar, N.S., Yalcin, S.E., Tuominen, M.T., and Lovley, D.R. (2014) Visulation of charge propagation along individual pili proteins using ambient electrostatatic force microscopy. Nat Nanotechnol Advance Online Publication. doi:10.1038/NNANO.2014.236.
45. Mehta, T., Childers, S.E., and Lovley, D. (2002) Geobacter sulfurreducens requires pili in order to reduce Fe(III) oxide. In Abstracts of the American Society of Microbiology 102nd General Meeting, Washington, DC: American Society for Microbiology, p. 410.
46. Melin, T., Zdrojek, M., and Brunel, D. (2010) Electrostatic force microscopy and Kelvin force microscopy as a probe of the electrostatic and electronic properties of carbon nanotubes. In Scanning Probe Microscopy in Nanoscience and Nanotechnology. Bhushan, B. (ed.). Berlin, Germany: Springer-Verlag, pp. 89-128.
47. Morita, M., Malvankar, N.S., Franks, A.E., Summers, Z.M., Giloteaux, L., Rotaru, A.E., etal. (2011) Potential for direct interspecies electron transfer in methanogenic wastewater digester aggregates. mBio 2: e00159-0011.
48. Näther, D.J., Rachel, R., Wanner, G., and Wirth, R. (2006) Flagella of Pyrococcus furiosus: multifunctional organelles, made for swimming, adhesion to various surfaces, and cell-cell contacts. J Bacteriol 188: 6915-6923.
49. Nevin, K.P., Kim, B.C., Glaven, R.H., Johnson, J.P., Woodard, T.L., Methé, B.A., etal. (2009) Anode biofilm transcriptomics reveals outer surface components essential for high density current production in Geobacter sulfurreducens fuel cells. PLoS ONE 4: e5628.
50. Nickell, S., Hegerl, R., Baumeister, W., and Rachel, R. (2003) Pyrodictium cannulae enter the periplasmic space but do not enter the cytoplasm, as revealed by cryo-electron tomography. J Struct Biol 141: 34-42.
51. Paillet, M., Poncharal, P., and Zahab, A. (2005) Electrostatics of individual single-walled carbon nanotubes investigated by electrostatic force microscopy. Phys Rev Lett 94: 186801.
52. Pirbadian, S., Barchinger, S.E., Leung, K.M., Byun, H.S., Jangir, Y., Bouhenni, R.A., etal. (2014) Shewanella oneidensis MR-1 nanowires are outer membrane and periplasmic extensions of the extracellular electron transport components. PNAS 111: 12883-12888.
53. Polizzi, N.F., Skourtis, S.S., and Beratan, D.N. (2012) Physical constraints on charge transport through bacterial nanowires. Faraday Discuss 155: 43-61.
54. Reardon, P.N., and Mueller, K.T. (2013) Structure of the type IVa major pilin from the electrically conductive bacterial nanowires of Geobacter sulfurreducens. J Biol Chem 288: 29260-29266.
55. Reguera, G., McCarthy, K.D., Mehta, T., Nicoll, J.S., Tuominen, M.T., and Lovley, D.R. (2005) Extracellular electron transfer via microbial nanowires. Nature 435: 1098-1101.
56. Reguera, G., Nevin, K.P., Nicoll, J.S., Covalla, S.F., Woodard, T.L., and Lovley, D.R. (2006) Biofilm and nanowire production leads to increased current in Geobacter sulfurreducens fuel cells. Appl Environ Microbiol 72: 7345-7348.
57. Remis, J.P., Wei, D., Gorur, A., Zemla, M., Haraga, J., Allen, S., etal. (2014) Bacterial social networks: structure and composition of Myxococcus xanthus outer membrane vesicle chains. Environ Microbiol 16: 598-610.
58. Rotaru, A.E., Shrestha, P.M., Liu, F., Markovaite, B., Chen, S., Nevin, K.P., and Lovley, D.R. (2014a) Direct interspecies electron transfer between Geobacter metallireducens and Methanosarcina barkeri. Appl Environ Microbiol 80: 4599-4605.
59. Rotaru, A.E., Shrestha, P.M., Liu, F., Shrestha, M., Shrestha, D., Embree, M., etal. (2014b) 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.
60. Shrestha, P.M., and Rotaru, A.-E. (2014) Plugging in or going wireless: strategies for interspecies electron transfer. Front Microbiol 5: 237.
61. Smith, K.S., and Ingram-Smith, C. (2007) Methanosaeta, the forgotten methanogen? Trends Microbiol 15: 150-155.
62. Smith, M.T.J., and Rubinstein, J.L. (2014) Beyond blob-ology. Science 345: 617-619.
63. Summers, Z.M., Fogarty, H.E., Leang, C., Franks, A.E., Malvankar, N.S., and Lovley, D.R. (2010) Direct exchange of electrons within aggregates of an evolved syntrophic coculture of anaerobic bacteria. Science 330: 1413-1415.
64. Vargas, M., Kashefi, K., Blunt-Harris, E.L., and Lovley, D.R. (1998) Microbiological evidence for Fe(III) reduction on early Earth. Nature 395: 65-67.
65. Vargas, M., Malvankar, N.S., Tremblay, P.L., Leang, C., Smith, J., Patel, P., etal. (2013) Aromatic amino acids required for pili conductivity and long-range extracellular electron transport in Geobacter sulfurreducens. mBio 4: e00105-00113.
66. Wanner, G., Vogl, K., and Overmann, J. (2008) Ultrastructural characterization of the prokaryotic symbiosis in 'Chlorochromatium aggregatum'. J Bacteriol 190: 3721-3730.
67. Yamada, C., Kato, S., Kimura, S., Ishii, M., and Igarashi, Y. (2014) Reduction of Fe(III) oxides by phylogenetically and physiologically diverse thermophilic methanogens. FEMS Microbiol Ecol 89: 637-645.
68. Yi, H., Nevin, K.P., Kim, B.C., Franks, A.E., Klimes, A., Tender, L.M., and Lovley, D.R. (2009) Selection of a variant of Geobacter sulfurreducens with enhanced capacity for current production in microbial fuel cells. Biosens Bioelectron 24: 3498-3503.
69. Zdrojek, M., Mélin, T., Diesinger, H., Stiévenard, D., Gebicki, W., and Adamowicz, L. (2006) Comment on 'electrostatics of individual single-walled carbon nanotubes investigated by electrostatic force microscopy. Phys Rev Lett 96: 039703.