Shewanella oneidensis MR-1 nanowires are outer membrane and periplasmic extensions of the extracellular electron transport components

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 35, 2014, Pages 12883-12888

  Pirbadian, Sahand ^a   Barchinger, Sarah E ^b   Leung, Kar Man ^a   Byun, Hye Suk ^a   Jangir, Yamini ^a   Bouhenni, Rachida A ^c   Reed, Samantha B ^d   Romine, Margaret F ^d   Saffarini, Daad A ^c   Shi, Liang ^d   Gorby, Yuri A ^e   Golbeck, John H ^b   El Naggar, Mohamed Y ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

^d PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

^e RENSSELAER POLYTECHNIC INSTITUTE   (United States)

Author keywords

Bioelectronics |; Extracellular electron transfer |; Membrane cytochromes; Respiration |

Indexed keywords

BIOELECTRONICS; EXTRACELLULAR ELECTRON TRANSFER; MEMBRANE CYTOCHROMES; RESPIRATION;

BACTERIAL OUTER MEMBRANE PROTEINS; BIOFUELS; CYTOCHROME C GROUP; ELECTRON TRANSPORT; GENE EXPRESSION REGULATION, BACTERIAL; MICROSCOPY, ATOMIC FORCE; MODELS, CHEMICAL; NANOWIRES; OXIDATION-REDUCTION; PERIPLASM; SHEWANELLA;

EID: 84907227973     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1410551111     Document Type: Article

References (43)

1. Gray HB, Winkler JR (2003) Electron tunneling through proteins. Q Rev Biophys 36(3):341-372.
2. Myers CR, Nealson KH (1988) Bacterial manganese reduction and growth with manganese oxide as the sole electron acceptor. Science 240(4857):1319-1321.
3. Nealson KH, Belz A, McKee B (2002) Breathing metals as a way of life: Geobiology in action. Antonie van Leeuwenhoek 81(1-4):215-222.
4. Kowalchuk GA, Jones SE, Blackall LL (2008) Microbes orchestrate life on Earth. ISME J 2(8):795-796.
5. El-Naggar MY, Finkel SE (2013) Live wires. Scientist 27(5):38-43.
6. Reguera G, et al. (2005) Extracellular electron transfer via microbial nanowires. Nature 435(7045):1098-1101.
7. Gorby YA, et al. (2006) Electrically conductive bacterial nanowires produced by Shewanella oneidensis strain MR-1 and other microorganisms. Proc Natl Acad Sci USA 103(30):11358-11363.
8. Marsili E, et al. (2008) Shewanella secretes flavins that mediate extracellular electron transfer. Proc Natl Acad Sci USA 105(10):3968-3973.
9. von Canstein H, Ogawa J, Shimizu S, Lloyd JR (2008) Secretion of flavins by Shewanella species and their role in extracellular electron transfer. Appl Environ Microbiol 74(3):615-623.
10. El-Naggar MY, et al. (2010) Electrical transport along bacterial nanowires from Shewanella oneidensis MR-1. Proc Natl Acad Sci USA 107(42):18127-18131.
11. Malvankar NS, et al. (2011) Tunable metallic-like conductivity in microbial nanowire networks. Nat Nanotechnol 6(9):573-579.
12. Pfeffer C, et al. (2012) Filamentous bacteria transport electrons over centimetre distances. Nature 491(7423):218-221.
13. Snider RM, Strycharz-Glaven SM, Tsoi SD, Erickson JS, Tender LM (2012) Long-range electron transport in Geobacter sulfurreducens biofilms is redox gradient-driven. Proc Natl Acad Sci USA 109(38):15467-15472.
14. Rabaey K, Rozendal RA (2010) Microbial electrosynthesis - revisiting the electrical route for microbial production. Nat Rev Microbiol 8(10):706-716.
15. Vargas M, et al. (2013) Aromatic amino acids required for pili conductivity and long-range extracellular electron transport in Geobacter sulfurreducens. MBio 4(2):e00105-e00113.
16. Strycharz-Glaven SM, Tender LM (2012) Reply to the 'Comment on "On electrical conductivity of microbial nanowires and biofilms"' by N. S. Malvankar, M. T. Tuominen and D. R. Lovley. Energy Environ Sci 5(3):6250-6255.
17. Pirbadian S, El-Naggar MY (2012) Multistep hopping and extracellular charge transfer in microbial redox chains. Phys Chem Chem Phys 14(40):13802-13808.
18. Polizzi NF, Skourtis SS, Beratan DN (2012) Physical constraints on charge transport through bacterial nanowires. Faraday Discuss 155:43-62, discussion 103-114.
19. Gorby Y, et al. (2008) Redox-reactive membrane vesicles produced by Shewanella. Geobiology 6(3):232-241.
20. Grossart HP, Steward GF, Martinez J, Azam F (2000) A simple, rapid method for demonstrating bacterial flagella. Appl Environ Microbiol 66(8):3632-3636.
21. Jones LJ, Haugland RP, Singer VL (2003) Development and characterization of the NanoOrange protein quantitation assay: A fluorescence-based assay of proteins in solution. Biotechniques 34(4):850-854, 856, 858 passim.
22. Leung KM, et al. (2011) Bacterial nanowires: Conductive as silicon, soft as polymer. Soft Matter 7(14):6617-6621.
23. El-Naggar MY, Gorby YA, Xia W, Nealson KH (2008) The molecular density of states in bacterial nanowires. Biophys J 95(1):L10-L12.
24. Leung KM, et al. (2013) Shewanella oneidensis MR-1 bacterial nanowires exhibit p-type, tunable electronic behavior. Nano Lett 13(6):2407-2411.
25. Kalyuzhnaya MG, Lidstrom ME, Chistoserdova L (2008) Real-time detection of actively metabolizing microbes by redox sensing as applied to methylotroph populations in Lake Washington. ISME J 2(7):696-706.
26. Cologgi DL, Lampa-Pastirk S, Speers AM, Kelly SD, Reguera G (2011) Extracellular reduction of uranium via Geobacter conductive pili as a protective cellular mechanism. Proc Natl Acad Sci USA 108(37):15248-15252.
27. Gray DR, Yue S, Chueng C-Y, Godfrey W (2005) Bacterial vitality detected by a novel fluorogenic redox dye using flow cytometry. Abstracts of the American Society of Microbiology Meeting (Am Soc Microbiol, Washington, DC).
28. Gralnick JA, Vali H, Lies DP, Newman DK (2006) Extracellular respiration of dimethyl sulfoxide by Shewanella oneidensis strain MR-1. Proc Natl Acad Sci USA 103(12):4669-4674.
29. Betz WJ, Mao F, Smith CB (1996) Imaging exocytosis and endocytosis. Curr Opin Neurobiol 6(3):365-371.
30. Bolte S, et al. (2004) FM-dyes as experimental probes for dissecting vesicle trafficking in living plant cells. J Microsc 214(Pt 2):159-173.
31. Griffing LR (2008) FRET analysis of transmembrane flipping of FM4-64 in plant cells: Is FM4-64 a robust marker for endocytosis? J Microsc 231(2):291-298.
32. Rosu V, Hughes KT (2006) sigma28-dependent transcription in Salmonella enterica is independent of flagellar shearing. J Bacteriol 188(14):5196-5203.
33. Blair KM, Turner L, Winkelman JT, Berg HC, Kearns DB (2008) A molecular clutch disables flagella in the Bacillus subtilis biofilm. Science 320(5883):1636-1638.
34. Lowenthal AC, et al. (2009) Functional analysis of the Helicobacter pylori flagellar switch proteins. J Bacteriol 191(23):7147-7156.
35. Luo Q, Dong Y, Chen H, Gao H (2013) Mislocalization of Rieske protein PetA predominantly accounts for the aerobic growth defect of Tat mutants in Shewanella oneidensis. PLoS ONE 8(4):e62064.
36. Rhodius VA, Gross CA (2011) Using DNA microarrays to assay part function. Methods Enzymol 497:75-113.
37. Bouhenni RA, et al. (2010) The role of Shewanella oneidensis MR-1 outer surface structures in extracellular electron transfer. Electroanalysis 22(7-8):856-864.
38. Howard EC, Petersen ER, Fitzgerald LA, Sheehan PE, Ringeisen BR (2011) Optimal method for efficiently removing extracellular nanofilaments from Shewanella oneidensis MR-1. J Microbiol Methods 87(3):320-324.
39. Clarke TA, et al. (2011) Structure of a bacterial cell surface decaheme electron conduit. Proc Natl Acad Sci USA 108(23):9384-9389.
40. Reardon CL, et al. (2010) Role of outer-membrane cytochromes MtrC and OmcA in the biomineralization of ferrihydrite by Shewanella oneidensis MR-1. Geobiology 8(1):56-68.
41. Kulp A, Kuehn MJ (2010) Biological functions and biogenesis of secreted bacterial outer membrane vesicles. Annu Rev Microbiol 64:163-184.
42. Remis JP, et al. (2014) Bacterial social networks: Structure and composition of Myxococcus xanthus outer membrane vesicle chains. Environ Microbiol 16(2):598-610.
43. Wanner G, Vogl K, Overmann J (2008) Ultrastructural characterization of the prokaryotic symbiosis in "Chlorochromatium aggregatum" J Bacteriol 190(10):3721-3730.