35. Harris HW, El-Naggar MY, Nealson KH (2012) Shewanella oneidensis MR-1 chemotaxis
proteins and electron-transport chain components essential for congregation near insoluble
electron acceptors. Biochem Soc Trans 40:1167–1177. https://doi.org/10.1042/
BST20120232
36. Lovley DR (2008) Extracellular electron transfer: wires, capacitors, iron lungs, and more.
Geobiology 6:225–231. https://doi.org/10.1111/j.1472-4669.2008.00148.x
37. El-Naggar MY, Wanger G, Leung KM, Yuzvinsky TD, Southam G, Yang J, Lau WM,
Nealson KH, Gorby YA (2010) Electrical transport along bacterial nanowires from
Shewanella oneidensis MR-1. Proc Natl Acad Sci 107:18127–18131. https://doi.org/10.
1073/pnas.1004880107
38. Gorby YA, Yanina S, Mclean JS, Rosso KM, Moyles D, Dohnalkova A, Beveridge TJ,
Chang IS, Kim BH, Kim KS, Culley DE, Reed SB, Romine MF, Saffarini DA, Hill EA,
Shi L, Elias DA, Kennedy DW, Pinchuk G, Watanabe K, Ishii S, Logan B, Nealson KH,
Fredrickson JK (2006) Electrically conductive bacterial nanowires produced by Shewanella
oneidensis strain MR-1 and other microorganisms. Proc Natl Acad Sci 103(30):11358–
11363. https://doi.org/10.1073/pnas.0604517103
39. Vargas M, Malvankar NS, Tremblay P, Leang C, Smith JA, Patel P, Synoeyenbos-West O,
Nevin KP, Lovley DR (2013) Aromatic amino acids required for Pili conductivity and
long-range extracellular electron transport in Geobacter sulfurreducens. MBio 4:1–6. https://
doi.org/10.1128/mBio.00105-13
40. Shi L, Deng S, Marshall MJ, Wang Z, Kennedy DW, Dohnalkova AC, Mottaz HM, Hill EA,
Gorby YA, Beliaev AS, Richardson DJ, Zachara JM, Fredrickson JK (2008) Direct
involvement of type II secretion system in extracellular translocation of Shewanella
oneidensis outer membrane cytochromes MtrC and OmcA. J Bacteriol 190:5512–5516.
https://doi.org/10.1128/JB.00514-08
41. Bouhenni RA, Vora GJ, Biffinger JC, Shirodkar S, Brockman K, Ray R, Wu P, Johnson BJ,
Biddle EM, Marshall MJ, Fitzgerald LA, Little BJ, Fredrickson JK, Beliaev AS,
Ringeisen BR, Saffarini DA (2010) The Role of Shewanella oneidensis MR-1 outer surface
structures in extracellular electron transfer. Electroanalysis 22:856–864. https://doi.org/10.
1002/elan.200880006
42. Pirbadian S, Barchinger SE, Leung KM, Byun HS, Jangir Y, Bouhenni RA, Reed SB,
Romine MF, Saffarini DA, Shi L, Gorby YA, Golbeck JH, El-Naggar MY (2014)
Shewanella oneidensis MR-1 nanowires are outer membrane and periplasmic extensions of
the extracellular electron transport components. Proc Natl Acad Sci 111:12883–12888.
https://doi.org/10.1073/pnas.1410551111
43. Holmes DE, Dang Y, Walker DJF, Lovley DR (2016) The electrically conductive pili of
Geobacter species are a recently evolved feature for extracellular electron transfer. Microb
Genomics 2:e000072. https://doi.org/10.1099/mgen.0.000072
44. Wang F, Gu Y, O’Brien JP, Yi SM, Yalcin SE, Srikanth V, Shen C, Vu D, Ing NL,
Hochbaum AI, Egelman EH, Malvankar NS (2019) Structure of microbial nanowires reveals
stacked hemes that transport electrons over micrometers. Cell 177:361-369.e10. https://doi.
org/10.1016/j.cell.2019.03.029
45. Filman DJ, Marino SF, Ward JE, Yang L, Mester Z, Bullitt E, Lovley DR, Strauss M (2019)
Cryo-EM reveals the structural basis of long-range electron transport in a cytochrome-based
bacterial nanowire. Commun Biol 2:219. https://doi.org/10.1038/s42003-019-0448-9
46. Childers SE, Ciufo S, Lovley DR (2002) Geobacter metallireducens accesses insoluble Fe
(iii) oxide by chemotaxis. Nature 416:767–769. https://doi.org/10.1038/416767a
47. 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. https://doi.org/10.1128/AEM.01444-06
48. 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. https://doi.org/10.1074/jbc.M113.498527
236
B. M. Fonseca et al.
proteins and electron-transport chain components essential for congregation near insoluble
electron acceptors. Biochem Soc Trans 40:1167–1177. https://doi.org/10.1042/
BST20120232
36. Lovley DR (2008) Extracellular electron transfer: wires, capacitors, iron lungs, and more.
Geobiology 6:225–231. https://doi.org/10.1111/j.1472-4669.2008.00148.x
37. El-Naggar MY, Wanger G, Leung KM, Yuzvinsky TD, Southam G, Yang J, Lau WM,
Nealson KH, Gorby YA (2010) Electrical transport along bacterial nanowires from
Shewanella oneidensis MR-1. Proc Natl Acad Sci 107:18127–18131. https://doi.org/10.
1073/pnas.1004880107
38. Gorby YA, Yanina S, Mclean JS, Rosso KM, Moyles D, Dohnalkova A, Beveridge TJ,
Chang IS, Kim BH, Kim KS, Culley DE, Reed SB, Romine MF, Saffarini DA, Hill EA,
Shi L, Elias DA, Kennedy DW, Pinchuk G, Watanabe K, Ishii S, Logan B, Nealson KH,
Fredrickson JK (2006) Electrically conductive bacterial nanowires produced by Shewanella
oneidensis strain MR-1 and other microorganisms. Proc Natl Acad Sci 103(30):11358–
11363. https://doi.org/10.1073/pnas.0604517103
39. Vargas M, Malvankar NS, Tremblay P, Leang C, Smith JA, Patel P, Synoeyenbos-West O,
Nevin KP, Lovley DR (2013) Aromatic amino acids required for Pili conductivity and
long-range extracellular electron transport in Geobacter sulfurreducens. MBio 4:1–6. https://
doi.org/10.1128/mBio.00105-13
40. Shi L, Deng S, Marshall MJ, Wang Z, Kennedy DW, Dohnalkova AC, Mottaz HM, Hill EA,
Gorby YA, Beliaev AS, Richardson DJ, Zachara JM, Fredrickson JK (2008) Direct
involvement of type II secretion system in extracellular translocation of Shewanella
oneidensis outer membrane cytochromes MtrC and OmcA. J Bacteriol 190:5512–5516.
https://doi.org/10.1128/JB.00514-08
41. Bouhenni RA, Vora GJ, Biffinger JC, Shirodkar S, Brockman K, Ray R, Wu P, Johnson BJ,
Biddle EM, Marshall MJ, Fitzgerald LA, Little BJ, Fredrickson JK, Beliaev AS,
Ringeisen BR, Saffarini DA (2010) The Role of Shewanella oneidensis MR-1 outer surface
structures in extracellular electron transfer. Electroanalysis 22:856–864. https://doi.org/10.
1002/elan.200880006
42. Pirbadian S, Barchinger SE, Leung KM, Byun HS, Jangir Y, Bouhenni RA, Reed SB,
Romine MF, Saffarini DA, Shi L, Gorby YA, Golbeck JH, El-Naggar MY (2014)
Shewanella oneidensis MR-1 nanowires are outer membrane and periplasmic extensions of
the extracellular electron transport components. Proc Natl Acad Sci 111:12883–12888.
https://doi.org/10.1073/pnas.1410551111
43. Holmes DE, Dang Y, Walker DJF, Lovley DR (2016) The electrically conductive pili of
Geobacter species are a recently evolved feature for extracellular electron transfer. Microb
Genomics 2:e000072. https://doi.org/10.1099/mgen.0.000072
44. Wang F, Gu Y, O’Brien JP, Yi SM, Yalcin SE, Srikanth V, Shen C, Vu D, Ing NL,
Hochbaum AI, Egelman EH, Malvankar NS (2019) Structure of microbial nanowires reveals
stacked hemes that transport electrons over micrometers. Cell 177:361-369.e10. https://doi.
org/10.1016/j.cell.2019.03.029
45. Filman DJ, Marino SF, Ward JE, Yang L, Mester Z, Bullitt E, Lovley DR, Strauss M (2019)
Cryo-EM reveals the structural basis of long-range electron transport in a cytochrome-based
bacterial nanowire. Commun Biol 2:219. https://doi.org/10.1038/s42003-019-0448-9
46. Childers SE, Ciufo S, Lovley DR (2002) Geobacter metallireducens accesses insoluble Fe
(iii) oxide by chemotaxis. Nature 416:767–769. https://doi.org/10.1038/416767a
47. 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. https://doi.org/10.1128/AEM.01444-06
48. 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. https://doi.org/10.1074/jbc.M113.498527
236
B. M. Fonseca et al.