1887

Chapter 5.2.1 : Breathing Iron: Molecular Mechanism of Microbial Iron Reduction by

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in
Zoomout

Breathing Iron: Molecular Mechanism of Microbial Iron Reduction by , Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555818821/9781555818821.ch5.2.1-1.gif /docserver/preview/fulltext/10.1128/9781555818821/9781555818821.ch5.2.1-2.gif

Abstract:

Dissimilatory Fe(III)-reducing bacteria occupy a central position in a variety of environmentally important processes, including the biogeochemical cycling of carbon and iron, the bioremediation of radionuclides and organohalides, and the generation of electricity in microbial fuel cells. Fe(III)-reducing bacteria are scattered and deeply rooted throughout both prokaryotic domains, an indication that microbial Fe(III) reduction may also have been one of the first respiratory processes to have evolved on early Earth. The metal-reducing γ-proteobacterium Shewanella oneidensis is one of the most extensively studied Fe(III)-reducing bacteria. This chapter examines the molecular mechanism by which S. oneidensis transfers electrons to Fe(III) ranging from highly soluble organic-Fe(III) complexes to highly insoluble Fe(III) oxides. S. oneidensis employs four novel respiratory pathways for dissimilatory Fe(III) reduction, including: i) localization of c-type cytochromes to the cell surface where they deliver electrons to external Fe(III) (Mechanism No. 1, Direct contact by outer membrane-localized c-type cytochromes); ii) localization of c-type cytochromes along extracellular nanowires where they deliver electrons to external Fe(III) (Mechanism No. 2, Direct contact by nanowire-localized c-type cytochromes); iii) delivery of electrons to external Fe(III) via endogenous or exogenous electron shuttles (Mechanism No. 3, Extracellular electron shuttling); and iv) non-reductive dissolution of Fe(III) oxides to form more readily reducible soluble organic-Fe(III) complexes (Mechanism No. 4, Fe(III) oxide solubilization followed by reduction of the produced soluble organic-Fe(III) complexes); The chapter highlights the mechanistic details associated with each of the four Fe(III) reduction pathways of S. oneidensis, including a concluding discussion of the future research directions for each pathway.

Citation: Cooper R, Goff J, Reed B, Sekar R, DiChristina T. 2016. Breathing Iron: Molecular Mechanism of Microbial Iron Reduction by , p 5.2.1-1-5.2.1-13. In Yates M, Nakatsu C, Miller R, Pillai S (ed), Manual of Environmental Microbiology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555818821.ch5.2.1
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Image of FIGURE 1
FIGURE 1

Working model for type II protein secretion-linked, direct enzymatic reduction of solid Fe(III)-oxides at the outer membrane. doi: 10.1128/9781555818821.ch5.2.1.f1

Citation: Cooper R, Goff J, Reed B, Sekar R, DiChristina T. 2016. Breathing Iron: Molecular Mechanism of Microbial Iron Reduction by , p 5.2.1-1-5.2.1-13. In Yates M, Nakatsu C, Miller R, Pillai S (ed), Manual of Environmental Microbiology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555818821.ch5.2.1
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2
FIGURE 2

Working model for electron transfer to solid Fe(III)-oxides via nanowires. doi: 10.1128/9781555818821.ch5.2.1.f2

Citation: Cooper R, Goff J, Reed B, Sekar R, DiChristina T. 2016. Breathing Iron: Molecular Mechanism of Microbial Iron Reduction by , p 5.2.1-1-5.2.1-13. In Yates M, Nakatsu C, Miller R, Pillai S (ed), Manual of Environmental Microbiology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555818821.ch5.2.1
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 3
FIGURE 3

Working model for electron shuttling pathway with AQDS as electron shuttle. doi: 10.1128/9781555818821.ch5.2.1.f3

Citation: Cooper R, Goff J, Reed B, Sekar R, DiChristina T. 2016. Breathing Iron: Molecular Mechanism of Microbial Iron Reduction by , p 5.2.1-1-5.2.1-13. In Yates M, Nakatsu C, Miller R, Pillai S (ed), Manual of Environmental Microbiology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555818821.ch5.2.1
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 4
FIGURE 4

Working model for Fe(III) solubilization-reduction pathway with endogenous organic ligand as Fe(III)-chelating compound. doi: 10.1128/9781555818821.ch5.2.1.f4

Citation: Cooper R, Goff J, Reed B, Sekar R, DiChristina T. 2016. Breathing Iron: Molecular Mechanism of Microbial Iron Reduction by , p 5.2.1-1-5.2.1-13. In Yates M, Nakatsu C, Miller R, Pillai S (ed), Manual of Environmental Microbiology, Fourth Edition. ASM Press, Washington, DC. doi: 10.1128/9781555818821.ch5.2.1
Permissions and Reprints Request Permissions
Download as Powerpoint

References

/content/book/10.1128/9781555818821.ch5.2.1
1. Logan BE. 2009. Exoelectrogenic bacteria that power microbial fuel cells. Nat Rev Microbiol 7( 5) : 375 381, doi: 10.1038/Nrmicro2113.[PubMed][CrossRef] http://dx.doi.org/10.1038/Nrmicro2113
2. Lovley DR,, Holmes DE,, Nevin KP. 2004. Dissimilatory Fe(III) and Mn(IV) reduction. Adv Microb Physiol 49 : 219 286.[PubMed][CrossRef]
3. Thamdrup B,. 2000. Bacterial manganese and iron reduction in aquatic sediments, p. 86 103. In Schink B ( ed.), Advances in Microbial Ecology. Kluwer Academic, Dordrecht.
4. Lovley DR,, Coates JD. 1997. Bioremediation of metal contamination. Curr Opin Biotechnol 8( 3) : 285 289.[PubMed][CrossRef]
5. Lonergan DJ,, Jenter HL,, Coates JD,, Phillips EJP,, Schmidt TM,, Lovley DR. 1996. Phylogenetic analysis of dissimilatory Fe(III)-reducing bacteria. J Bacteriol 178( 8) : 2402 2408.[PubMed]
6. Vargas M,, Kashefi K,, Blunt-Harris EL,, Lovley DR. 1998. Microbiological evidence for Fe(III) reduction on early Earth. Nature 395( 6697) : 65 67.[PubMed][CrossRef]
7. DiChristina TJ,, Moore CM,, Haller CA. 2002. Dissimilatory Fe(III) and Mn(IV) reduction by Shewanella putrefaciens requires ferE, a homolog of the pulE ( gspE) type II protein secretion gene. J Bacteriol 184( 1) : 142 151.[PubMed][CrossRef]
8. 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. U.S.A. 103( 30) : 11358 11363. doi: 10.1073/Pnas.0604517103.[PubMed][CrossRef] http://dx.doi.org/10.1073/Pnas.0604517103
9. Myers CR,, Myers JM. 1992. Localization of cytochromes to the outer-membrane of anaerobically grown Shewanella putrefaciens MR-1. J Bacteriol 174( 11) : 3429 3438.[PubMed]
10. Marsili E,, Baron DB,, Shikhare ID,, Coursolle D,, Gralnick JA,, Bond DR. 2008. Shewanella Ssecretes flavins that mediate extracellular electron transfer. Proc Natl Acad Sci USA. 105( 10) : 3968 3973.[PubMed][CrossRef]
11. Hernandez ME,, Kappler A,, Newman DK. 2004. Phenazines and other redox-active antibiotics promote microbial mineral reduction. Appl Environ Microbiol 70( 2) : 921 928.[PubMed][CrossRef]
12. Roden EE,, Kappler A,, Bauer I,, Paul A,, Jiang J,, Stoesser R,, Konishi H,, Xu H. 2010. Extracellular electron transfer through microbial reduction of solid-phase humic substances. Nat Geosci 3( 6) : 417 421.[CrossRef]
13. Fennessey CM,, Jones ME,, Taillefert M,, DiChristina TJ. 2010. Siderophores are not involved in Fe(III) solubilization during anaerobic Fe(III) respiration by Shewanella oneidensis MR-1. Appl Environ Microbiol 76( 8) : 2425 2432. doi: 10.1128/Aem.03066–09.[PubMed][CrossRef] http://dx.doi.org/10.1128/Aem.03066–09
14. Taillefert M,, Beckler JS,, Carey E,, Burns JL,, Fennessey CM,, DiChristina TJ. 2007. Shewanella putrefaciens produces an Fe(III)-solubilizing organic ligand during anaerobic respiration on insoluble Fe(III) oxides. J Inorg Biochem 101( 11–12) : 1760 1767.[PubMed][CrossRef]
15. Jones ME,, Fennessey CM,, DiChristina TJ,, Taillefert M. 2010. Shewanella oneidensis MR-1 mutants selected for their inability to produce soluble organic-Fe(III) complexes are unable to respire Fe(III) as anaerobic electron acceptor. Environ Microbiol 12( 4) : 938 950. doi: 10.1111/J.1462-2920.2009.02137.X.[PubMed][CrossRef] http://dx.doi.org/10.1111/J.1462-2920.2009.02137.X
16. Myers CR,, Myers JM. 1997. Cloning and sequence of cymA a gene encoding a tetraheme cytochrome c required for reduction of iron(III), fumarate, and nitrate by Shewanella putrefaciens MR-1. J Bacteriol 179( 4) : 1143 1152.[PubMed]
17. Schuetz B,, Schicklberger M,, Kuermann J,, Spormann AM,, Gescher J. 2009. Periplasmic electron transfer via the c-type cytochromes MtrA and FccA of Shewanella oneidensis MR-1. Appl Environ Microbiol 75( 24) : 7789 7796.[PubMed][CrossRef]
18. Beliaev AS,, Saffarini DA. 1998. Shewanella putrefaciens mtrB encodes an outer membrane protein required for Fe(III) and Mn(IV) reduction. J Bacteriol 180( 23) : 6292 6297.[PubMed]
19. Myers CR,, Myers JM. 2002. MtrB is required for proper incorporation of the cytochromes OmcA and OmcB into the outer membrane of Shewanella putrefaciens MR-1. Appl Environ Microbiol 68( 11) : 5585 5594.[PubMed][CrossRef]
20. Shi L,, Chen BW,, Wang Z,, Elias DA,, Mayer MU,, Gorby YA,, Ni S,, Lower BH,, Kennedy DW,, Wunschel DS,, Mottaz HM,, Marshall MJ,, Hill EA,, Beliaev AS,, Zachara JM,, Fredrickson JK,, Squier TC. 2006. Isolation of a high-affinity functional protein complex between OmcA and MtrC: Two outer membrane decaheme c-type cytochromes of Shewanella oneidensis MR-1. J Bacteriol 188( 13) : 4705 4714. doi: 10.1128/Jb.01966–05.[PubMed][CrossRef] http://dx.doi.org/10.1128/Jb.01966–05
21. Ross DE,, Ruebush SS,, Brantley SL,, Hartshorne RS,, Clarke TA,, Richardson DJ,, Tien M. 2007. Characterization of protein-protein interactions involved in iron reduction by Shewanella oneidensis MR-1. Appl Environ Microbiol 73( 18) : 5797 5808.[PubMed][CrossRef]
22. Eggleston CM,, Voros J,, Shi L,, Lower BH,, Droubay TC,, Colberg PJS. 2008. Binding and direct electrochemistry of OmcA, an outer-membrane cytochrome from an iron reducing bacterium, with oxide electrodes: a candidate biofuel cell system. Inorg Chim Acta 361( 3) : 769 777. doi: 10.1016/J.Ica.2007.07.015.[CrossRef] http://dx.doi.org/10.1016/J.Ica.2007.07.015
23. Hartshorne RS,, Jepson BN,, Clarke TA,, Field SJ,, Fredrickson J,, Zachara J,, Shi L,, Butt JN,, Richardson DJ. 2007. Characterization of Shewanella oneidensis MtrC: a cell-surface decaheme cytochrome involved in respiratory electron transport to extracellular electron acceptors. J Biol Inorg Chem 12( 7) : 1083 1094. doi: 10.1007/S00775-007-0278-Y.[PubMed][CrossRef] http://dx.doi.org/10.1007/S00775-007-0278-Y
24. Richardson DJ,, Butt JN,, Fredrickson JK,, Zachara JM,, Shi L,, Edwards MJ,, White G,, Baiden N,, Gates AJ,, Marritt SJ,, Clarke TA. 2012. The porin-cytochrome' model for microbe-to-mineral electron transfer. Mol Microbiol 85( 2) : 201 212.[PubMed][CrossRef]
25. Hartshorne RS,, Reardon CL,, Ross D,, Nuester J,, Clarke TA,, Gates AJ,, Mills PC,, Fredrickson JK,, Zachara JM,, Shi L,, Beliaev AS,, Marshall MJ,, Tien M,, Brantley S,, Butt JN,, Richardson DJ. 2009. Characterization of an electron conduit between bacteria and the extracellular environment. Proc Natl Acad Sci USA 106( 52) : 22169 22174. doi: 10.1073/Pnas.0900086106.[PubMed][CrossRef] http://dx.doi.org/10.1073/Pnas.0900086106
26. White GF,, Shi Z,, Shi L,, Wang ZM,, Dohnalkova AC,, Marshall MJ,, Fredrickson JK,, Zachara JM,, Butt JN,, Richardson DJ,, Clarke TA. 2013. Rapid electron exchange between surface-exposed bacterial cytochromes and Fe(III) minerals. Proc Natl Acad Sci USA 110( 16) : 6346 6351.[PubMed][CrossRef]
27. Coursolle D,, Gralnick JA. 2010. Modularity of the Mtr respiratory pathway of Shewanella oneidensis strain MR-1. Mol Microbiol 77( 4) : 995 1008.[PubMed]
28. Firer-Sherwood MA,, Bewley KD,, Mock J-Y,, Elliott SJ. 2011. Tools for resolving complexity in the electron transfer networks of multiheme cytochromes c. Metallomics 3( 4) : 344 348.[PubMed][CrossRef]
29. Firer-Sherwood M,, Pulcu GS,, Elliott SJ. 2008. Electrochemical interrogations of the Mtr cytochromes from Shewanella: opening a potential window. J Biol Inorg Chem 13( 6) : 849 854.[PubMed][CrossRef]
30. Léger C,, Elliott SJ,, Hoke KR,, Jeuken LJ,, Jones AK,, Armstrong FA. 2003. Enzyme electrokinetics: using protein film voltammetry to investigate redox enzymes and their mechanisms. Biochemistry 42( 29) : 8653 8662.[PubMed][CrossRef]
31. Gescher JS,, Cordova CD,, Spormann AM. 2008. Dissimilatory iron reduction in Escherichia coli: identification of CymA of Shewanella oneidensis and NapC of E. coli as ferric reductases. Mol Microbiol 68( 3) : 706 719.[PubMed][CrossRef]
32. Marritt SJ,, Lowe TG,, Bye J,, Mcmillan DG,, Shi L,, Fredrickson J,, Zachara J,, Richardson DJ,, Cheesman MR,, Jeuken LJ,, Butt JN. 2012. A functional description of CymA, an electron-transfer hub supporting anaerobic respiratory flexibility in Shewanella. Biochem J 444( 3) : 465 474.[PubMed][CrossRef]
33. Marritt SJ,, Mcmillan DG,, Shi L,, Fredrickson JK,, Zachara JM,, Richardson DJ,, Jeuken LJ,, Butt JN. 2012. The roles of CymA in support of the respiratory flexibility of Shewanella oneidensis MR-1. Biochem Soc Trans 40( 6) : 1217.[PubMed][CrossRef]
34. Myers JM,, Myers CR. 2000. Role of the tetraheme cytochrome CymA in anaerobic electron transport in cells of Shewanella putrefaciens MR-1 with normal levels of menaquinone. J Bacteriol 182( 1) : 67 75.[PubMed][CrossRef]
35. Myers CR,, Myers JM. 1997. Cloning and sequence of cymA, a gene encoding a tetraheme cytochrome c required for reduction of iron (III), fumarate, and nitrate by Shewanella putrefaciens MR-1. J Bacteriol 179( 4) : 1143 1152.[PubMed]
36. Schwalb C,, Chapman SK,, Reid GA. 2003. The tetraheme cytochrome CymA is required for anaerobic respiration with dimethyl sulfoxide and nitrite in Shewanella oneidensis. Biochemistry 42( 31) : 9491 9497.[PubMed][CrossRef]
37. Murphy JN,, Saltikov CW. 2007. The cymA gene, encoding a tetraheme c-type cytochrome, is required for arsenate respiration in Shewanella species. J Bacteriol 189( 6) : 2283 2290.[PubMed][CrossRef]
38. Schwalb C,, Chapman SK,, Reid GA. 2002. The membrane-bound tetrahaem c-type cytochrome CymA interacts directly with the soluble fumarate reductase in Shewanella. Biochem Soc Trans 30( 4) : 658 662.[CrossRef]
39. Myers J,, Myers C. 2003. Overlapping role of the outer membrane cytochromes of Shewanella oneidensis MR-1 in the reduction of manganese (IV) oxide. Lett Appl Microbiol 37( 1) : 21 25.[PubMed][CrossRef]
40. Jiao Y,, Qian F,, Li Y,, Wang G,, Saltikov CW,, Gralnick JA. 2011. Deciphering the electron transport pathway for graphene oxide reduction by Shewanella oneidensis MR-1. J Bacteriol 193( 14) : 3662 3665.[PubMed][CrossRef]
41. Salas EC,, Sun Z,, Lüttge A,, Tour JM. 2010. Reduction of graphene oxide via bacterial respiration. ACS Nano 4( 8) : 4852 4856. doi: 10.1021/nn101081t.[PubMed][CrossRef] http://dx.doi.org/10.1021/nn101081t
42. Beliaev AS,, Saffarini DA,, McLaughlin JL,, Hunnicutt D. 2001. MtrC, an outer membrane decahaem c cytochrome required for metal reduction in Shewanella putrefaciens MR-1. Mol Microbiol 39( 3) : 722 730.[PubMed][CrossRef]
43. Pitts KE,, Dobbin PS,, Reyes-Ramirez F,, Thomson AJ,, Richardson DJ,, Seward HE. 2003. Characterization of the Shewanella oneidensis MR-1 decaheme cytochrome MtrA expression in Escherichia coli confers the ability to reduce soluble Fe (III) chelates. J Biol Chem 278( 30) : 27758 27765.[PubMed][CrossRef]
44. 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.[PubMed][CrossRef]
45. Bewley K,, FirerSherwood M,, Mock J,, Ando N,, Drennan C,, Elliott S. 2012. Mind the gap: diversity and reactivity relationships among multihaem cytochromes of the MtrA/DmsE family. Biochem Soc Trans 40( 6) : 1268.[PubMed][CrossRef]
46. Gao H,, Barua S,, Liang Y,, Wu L,, Dong Y,, Reed S,, Chen J,, Culley D,, Kennedy D,, Yang Y,, He Z,, Nealson KH,, Fredrickson JK,, Tiedje JM,, Romine M,, Zhou J. 2010. Impacts of Shewanella oneidensis c-type cytochromes on aerobic and anaerobic respiration. Microb Biotechnol 3( 4) : 455 466.[PubMed][CrossRef]
47. Fredrickson JK,, Romine MF,, Beliaev AS,, Auchtung JM,, Driscoll ME,, Gardner TS,, Nealson KH,, Osterman AL,, Pinchuk G,, Reed JL,, Rodionov DA,, Rodrigues JL,, Saffarini DA,, Serres MH,, Spormann AM,, Zhulin IB,, Tiedje JM. 2008. Towards environmental systems biology of Shewanella. Nat Rev Microbiol 6( 8) : 592 603.[PubMed][CrossRef]
48. Edwards M,, Fredrickson J,, Zachara J,, Richardson D,, Clarke T. 2012. Analysis of structural MtrC models based on homology with the crystal structure of MtrF. Biochem Soc Trans 40( 6) : 1181.[PubMed][CrossRef]
49. Clarke TA,, Edwards MJ,, Gates AJ,, Hall A,, White GF,, Bradley J,, Reardon CL,, Shi L,, Beliaev AS,, Marshall MJ,, Wang Z,, Watmough NJ,, Fredrickson JK,, Zachara JM,, Butt JN,, Richardson DJ. 2011. Structure of a bacterial cell surface decaheme electron conduit. Proc Natl Acad Sci 108( 23) : 9384 9389.[PubMed][CrossRef]
50. Wee SK,, Burns JL,, DiChristina TJ. 2014. Identification of a molecular signature unique to metal-reducing Gammaproteobacteria. FEMS Microbiol Lett 350( 1) : 90 99.[PubMed][CrossRef]
51. Myers JM,, Myers CR. 2001. Role for outer membrane cytochromes OmcA and OmcB of Shewanella putrefaciens MR-1 in reduction of manganese dioxide. Appl Environ Microbiol 67( 1) : 260 269.[PubMed][CrossRef]
52. Hau HH,, Gilbert A,, Coursolle D,, Gralnick JA. 2008. Mechanism and consequences of anaerobic respiration of cobalt by Shewanella oneidensis strain MR-1. Appl Environ Microbiol 74( 22) : 6880 6886.[PubMed][CrossRef]
53. Marshall MJ,, Plymale AE,, Kennedy DW,, Shi L,, Wang Z,, Reed SB,, Dohnalkova AC,, Simonson CJ,, Liu C,, Saffarini DA,, Romine MF,, Zachara JM,, Beliaev AS,, Fredrickson JK. 2008. Hydrogenase- and outer membrane c-type cytochrome-facilitated reduction of technetium (VII) by Shewanella oneidensis MR-1. Environ Microbiol 10( 1) : 125 136.[PubMed]
54. Marshall MJ,, Beliaev AS,, Dohnalkova AC,, Kennedy DW,, Shi L,, Wang Z,, Boyanov MI,, Lai B,, Kemner KM,, Mclean JS,, Reed SB,, Culley DE,, Bailey VL,, Simonson CJ,, Saffarini DA,, Romine MF,, Zachara JM,, Fredrickson JK. 2006. c-Type cytochrome-dependent formation of U (IV) nanoparticles by Shewanella oneidensis. PLoS Biol 4( 8) : e268.[PubMed][CrossRef]
55. Shi L,, Squier TC,, Zachara JM,, Fredrickson JK. 2007. Respiration of metal (hydr) oxides by Shewanella and Geobacter: a key role for multihaem c-type cytochromes. Mol Microbiol 65( 1) : 12 20.[PubMed][CrossRef]
56. Newton GJ,, Mori S,, Nakamura R,, Hashimoto K,, Watanabe K. 2009. Analyses of current-generating mechanisms of Shewanella loihica PV-4 and Shewanella oneidensis MR-1 in microbial fuel cells. Appl Environ Microbiol 75( 24) : 7674 7681.[PubMed][CrossRef]
57. Lower BH,, Yongsunthon R,, Shi L,, Wilding L,, Gruber HJ,, Wigginton NS,, Reardon CL,, Pinchuk GE,, Droubay TC,, Boily JF,, Lower SK. 2009. Antibody recognition force microscopy shows that outer membrane cytochromes OmcA and MtrC are expressed on the exterior surface of Shewanella oneidensis MR-1. Appl Environ Microbiol 75( 9) : 2931 2935.[PubMed][CrossRef]
58. Ross DE,, Brantley SL,, Tien M. 2009. Kinetic characterization of OmcA and MtrC, terminal reductases involved in respiratory electron transfer for dissimilatory iron reduction in Shewanella oneidensis MR-1. Appl Environ Microbiol 75( 16) : 5218 5226. doi: 10.1128/aem.00544-09.[PubMed][CrossRef] http://dx.doi.org/10.1128/aem.00544-09
59. Hartshorne RS,, Jepson BN,, Clarke TA,, Field SJ,, Fredrickson J,, Zachara J,, Shi L,, Butt JN,, Richardson DJ. 2007. Characterization of Shewanella oneidensis MtrC: a cell-surface decaheme cytochrome involved in respiratory electron transport to extracellular electron acceptors. J Biol Inorg Chem 12( 7) : 1083 1094.[PubMed][CrossRef]
60. Coursolle D,, Baron DB,, Bond DR,, Gralnick JA. 2010. The Mtr respiratory pathway is essential for reducing Flavins and electrodes in Shewanella oneidensis. J Bacteriol 192( 2) : 467 474.[PubMed][CrossRef]
61. Shi L,, Chen B,, Wang Z,, Elias DA,, Mayer MU,, Gorby YA,, Ni S,, Lower BH,, Kennedy DW,, Wunschel DS,, Mottaz HM,, Marshall MJ,, Hill EA,, Beliaev AS,, Zachara JM,, Fredrickson JK,, Squier TC. 2006. Isolation of a high-affinity functional protein complex between OmcA and MtrC: two outer membrane decaheme c-type cytochromes of Shewanella oneidensis MR-1. J Bacteriol 188( 13) : 4705 4714.[PubMed][CrossRef]
62. DiChristina TJ,, Moore CM,, Haller CA. 2002. Dissimilatory Fe (III) and Mn (IV) reduction by Shewanella putrefaciens requires ferE, a homolog of the pulE (gspE) type II protein secretion gene. J Bacteriol 184( 1) : 142 151.[PubMed][CrossRef]
63. 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( 15) : 5512 5516.[PubMed][CrossRef]
64. Mitchell AC,, Peterson L,, Reardon CL,, Reed SB,, Culley DE,, Romine MR,, Geesey GG. 2012. Role of outer membrane c-type cytochromes MtrC and OmcA in Shewanella oneidensis MR-1 cell production, accumulation, and detachment during respiration on hematite. Geobiology 10( 4) : 355 370.[PubMed][CrossRef]
65. Xiong Y,, Shi L,, Chen B,, Mayer MU,, Lower BH,, Londer Y,, Bose S,, Hochella MF,, Fredrickson JK,, Squier TC. 2006. High-affinity binding and direct electron transfer to solid metals by the Shewanella oneidensis MR-1 outer membrane c-type cytochrome OmcA. J Am Chem Soc 128( 43) : 13978 13979. doi: 10.1021/ja063526d.[PubMed][CrossRef] http://dx.doi.org/10.1021/ja063526d.
66. Fredrickson JK,, Zachara JM. 2008. Electron transfer at the microbe–mineral interface: a grand challenge in biogeochemistry. Geobiology 6( 3) : 245 253.[PubMed][CrossRef]
67. Meitl LA,, Eggleston CM,, Colberg PJ,, Khare N,, Reardon CL,, Shi L. 2009. Electrochemical interaction of Shewanella oneidensis MR-1 and its outer membrane cytochromes OmcA and MtrC with hematite electrodes. Geochim Cosmochim Acta 73( 18) : 5292 5307.[CrossRef]
68. Lower BH,, Shi L,, Yongsunthon R,, Droubay TC,, McCready DE,, Lower SK. 2007. Specific bonds between an iron oxide surface and outer membrane cytochromes MtrC and OmcA from Shewanella oneidensis MR-1. J Bacteriol 189( 13) : 4944 4952.[PubMed][CrossRef]
69. Reardon CL,, Dohnalkova AC,, Nachimuthu P,, Kennedy DW,, Saffarini DA,, Arey BW,, Shi L,, Wang Z,, Moore D,, Mclean JS,, Moyles D,, Marshall MJ,, Zachara JM,, Fredrickson JK,, Beliaev AS. 2010. Role of outer-membrane cytochromes MtrC and OmcA in the biomineralization of ferrihydrite by Shewanella oneidensis MR-1. Geobiology 8( 1) : 56 68.[PubMed][CrossRef]
70. Marsili E,, Baron DB,, Shikhare ID,, Coursolle D,, Gralnick JA,, Bond DR. 2008. Shewanella secretes flavins that mediate extracellular electron transfer. Proc Natl Acad Sci 105( 10) : 3968 3973.[PubMed][CrossRef]
71. Szeinbaum N,, Burns JL, DiChristina TJ. 2014. Electron transport and protein secretion pathways involved in Mn(III) reduction by Shewanella oneidensis. Environ Microbiol Rep 6( 5) : 490 500.[PubMed][CrossRef]
72. Richter K,, Schicklberger M,, Gescher J. 2012. Dissimilatory reduction of extracellular electron acceptors in anaerobic respiration. Appl Environ Microbiol 78( 4) : 913 921. doi: 10.1128/aem.06803-11.[PubMed][CrossRef] http://dx.doi.org/10.1128/aem.06803-11
73. Lovley DR. 1993. Dissimilatory metal reduction. Ann Rev Microbiol 47( 1) : 263 290.[CrossRef]
74. Gaboriaud F,, Bailet S,, Dague E,, Jorand F. 2005. Surface structure and nanomechanical properties of Shewanella putrefaciens bacteria at two pH values (4 and 10) determined by atomic force microscopy. J Bacteriol 187( 11) : 3864 3868.[PubMed][CrossRef]
75. Sokolov I,, Smith D,, Henderson G,, Gorby Y,, Ferris F. 2001. Cell surface electrochemical heterogeneity of the Fe (III)-reducing bacteria Shewanella putrefaciens. Environ Sci Technol 35( 2) : 341 347.[PubMed][CrossRef]
76. Lower SK,, Hochella MF,, Beveridge TJ. 2001. Bacterial recognition of mineral surfaces: nanoscale interactions between Shewanella and α-FeOOH. Science 292( 5520) : 1360 1363.[PubMed][CrossRef]
77. Roden EE. 2003. Fe (III) oxide reactivity toward biological versus chemical reduction. Environ Sci Technol 37( 7) : 1319 1324.[CrossRef]
78. Kerisit S,, Rosso KM,, Dupuis M,, Valiev M. 2007. Molecular computational investigation of electron-transfer kinetics across cytochrome-iron oxide interfaces. J Phys Chem 111( 30) : 11363 11375.
79. Leys D,, Meyer TE,, Tsapin AS,, Nealson KH,, Cusanovich MA,, Van Beeumen JJ. 2002. Crystal structures at atomic resolution reveal the Novel Concept of “Electron-harvesting” as a role for the small tetraheme cytochrome c. J Biol Chem 277( 38) : 35703 35711. doi: 10.1074/jbc.M203866200.[PubMed][CrossRef] http://dx.doi.org/10.1074/jbc.M203866200
80. Jani R,, Colberg P,, Eggleston C,, Shi L,, Reardon C. 2010. Microbial fuel cell study of the role of OmcA and MtrC in electron transfer from Shewanella oneidensis to oxide electrodes, p 290. In Goldschmidt Conference on Earth, Energy, and the Environment, Knoxville, TN.
81. Belchik SM,, Kennedy DW,, Dohnalkova AC,, Wang Y,, Sevinc PC,, Wu H,, Lin Y,, Lu HP,, Fredrickson JK,, Shi L. 2011. Extracellular reduction of hexavalent chromium by cytochromes MtrC and OmcA of Shewanella oneidensis MR-1. Appl Environ Microbiol 77( 12) : 4035 4041.[PubMed][CrossRef]
82. 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( 42) : 18127 18131.[PubMed][CrossRef]
83. Leung KM,, Wanger G,, El-Naggar M,, Gorby Y,, Southam G,, Lau WM,, Yang J. 2013. Shewanella oneidensis MR-1 bacterial nanowires exhibit P-type, tunable electronic behaviour. Nano Lett 13( 6) : 2407 2411.[PubMed][CrossRef]
84. Briseno AL,, Mannsfeld SC,, Jenekhe SA,, Bao Z,, Xia Y. 2008. Introducing organic nanowire transistors. Mater Today 11( 4) : 38 47.[CrossRef]
85. Lovley DR. 2008. Extracellular electron transfer: wires, capacitors, iron lungs, and more. Geobiology 6( 3) : 225 231.[PubMed][CrossRef]
86. Reguera G,, McCarthy KD,, Mehta T,, Nicoll JS,, Tuominen MT,, Lovley DR. 2005. Extracellular electron transfer via microbial nanowires. Nature 435( 7045) : 1098 1101.[PubMed][CrossRef]
87. 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( 7–8) : 856 864. doi: 10.1002/elan.200880006.[CrossRef] http://dx.doi.org/10.1002/elan.200880006
88. Fitzgerald LA,, Petersen ER,, Ray RI,, Little BJ,, Cooper CJ,, Howard EC,, Ringeisen BR,, Biffinger JC. 2012. Shewanella oneidensis MR-1 Msh pilin proteins are involved in extracellular electron transfer in microbial fuel cells. Proc Biochem 47( 1) : 170 174. doi: 10.1016/j.procbio.2011.10.029[CrossRef]
89. El-Naggar MY,, Gorby YA,, Xia W,, Nealson KH. 2008. The molecular density of states in bacterial nanowires. Biophys J 95( 1) : L10 L12.[PubMed][CrossRef]
90. 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 Nano 6( 9) : 573 579.[CrossRef]
91. Lovley DR. 2012. Electromicrobiology. Ann Rev Microbiol 66 : 391 409.[CrossRef]
92. Morita M,, Malvankar NS,, Franks AE,, Summers ZM,, Giloteaux L,, Rotaru AE,, Rotaru C,, Lovley DR. 2011. Potential for direct interspecies electron transfer in methanogenic wastewater digester aggregates. MBio 2( 4) : e00159-11.[PubMed][CrossRef]
93. Summers ZM,, Fogarty HE,, Leang C,, Franks AE,, Malvankar NS,, Lovley DR. 2010. Direct exchange of electrons within aggregates of an evolved syntrophic coculture of anaerobic bacteria. Science 330( 6009) : 1413 1415.[PubMed][CrossRef]
94. Ntarlagiannis D,, Atekwana EA,, Hill EA,, Gorby Y. 2007. Microbial nanowires: is the subsurface “hardwired”? Geophysical Res Lett 34( 17) : L17305.[CrossRef]
95. Polizzi NF,, Skourtis SS,, Beratan DN. 2012. Physical constraints on charge transport through bacterial nanowires. Faraday Discuss 155 : 43 61.[PubMed][CrossRef]
96. 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. doi: 10.1128/Aem.01387-07.[PubMed][CrossRef] http://dx.doi.org/10.1128/Aem.01387-07
97. Lies DP,, Hernandez ME,, Kappler A,, Mielke RE,, Gralnick JA,, Newman DK. 2005. Shewanella oneidensis MR-1 uses overlapping pathways for iron reduction at a distance and by direct contact under conditions relevant for biofilms. Appl Environ Microbiol 71( 8) : 4414 4426. doi: 10.1128/Aem.71.8.4414-4426.2005.[PubMed][CrossRef] http://dx.doi.org/10.1128/Aem.71.8.4414-4426.2005
98. Nevin KP,, Lovley DR. 2002. Mechanisms for Fe(III) oxide reduction in sedimentary environments. Geomicrobiol J 19( 2) : 141 159.[CrossRef]
99. Gorton L,, Lindgren A,, Larsson T,, Munteanu FD,, Ruzgas T,, Gazaryan I. 1999. Direct electron transfer between heme-containing enzymes and electrodes as a basis for third generation biosensors. Anal Chim Acta 400( 1) : 91 108.[CrossRef]
100. Freire RS,, Pessoa CA,, Mello LD,, Kubota LT. 2003. Direct electron transfer: an approach for electrochemical biosensors with higher selectivity and sensitivity. J Braz Chem Soc 14( 2) : 230 243.[CrossRef]
101. Gray HB,, Winkler JR. 1996. Electron transfer in proteins. Ann Rev Biochem 65 : 537 561.[PubMed][CrossRef]
102. Lovley DR,, Coates JD,, Blunt-Harris EL,, Phillips EJP,, Woodward JC. 1996. Humic substances as electron acceptors for microbial respiration. Nature 382( 6590) : 445 448.[CrossRef]
103. Myers CR,, Myers JA. 2004. Shewanella oneidensis MR-1 restores menaquinone synthesis to a menaquinone-negative mutant. Appl Environ Microbiol 70( 9) : 5415 5425. doi: 10.1128/Aem.70.9.5415-5425.2004.[PubMed][CrossRef] http://dx.doi.org/10.1128/Aem.70.9.5415-5425.2004
104. Newman DK,, Kolter R. 2000. A role for excreted quinones in extracellular electron transfer. Nature 405( 6782) : 94 97.[PubMed][CrossRef]
105. Nevin KP,, Lovley DR. 2000. Potential for nonenzymatic reduction of Fe(III) via electron shuttling in subsurface sediments. Environ Sci Technol 34( 12) : 2472 2478.[CrossRef]
106. Lovley DR,, Kashefi K,, Vargas M,, Tor JM,, Blunt-Harris EL. 2000. Reduction of humic substances and Fe(III) by hyperthermophilic microorganisms. Chem Geol 169( 3–4) : 289 298.[CrossRef]
107. Roden EE. 2012. Microbial iron-redox cycling in subsurface environments. Biochem Soc T 40 : 1249 1256.[CrossRef]
108. Roden EE,, Kappler A,, Bauer I,, Jiang J,, Paul A,, Stoesser R,, Konishi H,, Xu H. 2010. Extracellular electron transfer through microbial reduction of solid-phase humic substances. Nat Geosci 3( 6) : 417 421.[CrossRef]
109. Turick CE,, Tisa LS,, Caccavo F. 2002. Melanin production and use as a soluble electron shuttle for Fe(III) oxide reduction and as a terminal electron acceptor by Shewanella algae BrY. Appl Environ Microbiol 68( 5) : 2436 2444.[PubMed][CrossRef]
110. Shi Z,, Zachara JM,, Shi L,, Wang Z,, Moore DA,, Kennedy DW,, Fredrickson JK. 2012. Redox reactions of reduced flavin mononucleotide (FMN), riboflavin (RBF), and anthraquinone-2,6-disulfonate (AQDS) with ferrihydrite and lepidocrocite. Environ Sci Technol 46( 21) : 11644 11652.[PubMed][CrossRef]
111. Okamoto A,, Hashimoto K,, Nealson KH,, Nakamura R. Rate enhancement of bacterial extracellular electron transport involves bound flavin semiquinones. Proc Natl Acad Sci USA 110( 19) : 7856 7861.[CrossRef]
112. Lovley DR,, Phillips E,, Lonergan DJ,, Widman PK. 1995. Fe (III) and S0 reduction by Pelobacter carbinolicus. Appl Environ Microbiol 61( 6) : 2132 2138.[PubMed]
113. Millero FJ,, Yao WS,, Aicher J. 1955. The speciation of Fe(II) and Fe(III) in natural-waters. Mar Chem 50 : 21 39.[CrossRef]
114. Zinder B,, Furrer G,, Stumm W. 1986. Coordination chemistry of weathering kinetics of the surface. 2. Dissociation of Fe(III) oxides. Geochim Cosmochim Acta 50 : 1861 1869.[CrossRef]
115. DiChristina TJ,, Fredrickson JK,, Zachara JM. 2005. Enzymology of electron transport: energy generation with geochemical consequences. Rev Mineral Geochem 59 : 27 52. doi: 10.2138/Rmg.2005.59.3.[CrossRef] http://dx.doi.org/10.2138/Rmg.2005.59.3
116. Yang Y,, Harris DP,, Luo F,, Wu L,, Parsons AB,, Palumbo AV,, Zhou J. 2008. Characterization of the Shewanella oneidensis Fur gene: roles in iron and acid tolerance response. BMC Genomics 9( Suppl 1) : S11. doi: 10.1186/1471-2164-9-S1-S11.[PubMed][CrossRef] http://dx.doi.org/10.1186/1471-2164-9-S1-S11
117. Fennessey CM,, Jones ME,, Taillefert M,, DiChristina TJ. 2010. Siderophores are not involved in Fe(III) solubilization during anaerobic Fe(III) respiration by Shewanella oneidensis MR-1. Appl Environ Microbiol 76( 8) : 2425 2432. doi: 10.1128/AEM.03066-09.[PubMed][CrossRef] http://dx.doi.org/10.1128/AEM.03066-09
118. Laglera LM,, van den Berg CMG. 2009. Evidence for geochemical control of iron by humic substances in seawater. Limnol Oceanogr 54( 2) : 610 619. doi: 10.4319/Lo.2009.54.2.0610.[CrossRef] http://dx.doi.org/10.4319/Lo.2009.54.2.0610
119. Vraspir JM,, Butler A. 2009. Chemistry of marine ligands and siderophores. Ann Rev Mar Sci 1 : 43 63. doi: 10.1146/Annurev.Marine.010908.163712.[PubMed][CrossRef] http://dx.doi.org/10.1146/Annurev.Marine.010908.163712
120. Bennett SA,, Achterberg EP,, Connelly DP,, Statham PJ,, Fones GR,, German CR. 2008. The distribution and stabilisation of dissolved Fe in deep-sea hydrothermal plumes. Earth Planet Sci Lett 270( 3–4) : 157 167. doi: 10.1016/J.Epsl.2008.01.048.[CrossRef] http://dx.doi.org/10.1016/J.Epsl.2008.01.048
121. Toner BM,, Fakra SC,, Manganini SJ,, Santelli CM,, Marcus MA,, Moffett J,, Rouxel O,, German CR,, Edwards KJ. 2009. Preservation of iron(II) by carbon-rich matrices in a hydrothermal plume. Nat Geosci 2( 3) : 197 201. doi: 10.1038/Ngeo433.[CrossRef] http://dx.doi.org/10.1038/Ngeo433
122. Bruland KW,, Rue EL,, Smith GJ. 2001. Iron and macronutrients in California coastal upwelling regimes: implications for diatom blooms. Limnol Oceanogr 46( 7) : 1661 1674.[CrossRef]
123. Buck KN,, Lohan MC,, Berger CJM,, Bruland KW. 2007. Dissolved iron speciation in two distinct river plumes and an estuary:implications for riverine iron supply. Limnol Oceanogr 52( 2) : 843 855.[CrossRef]
124. Gerringa LJA,, Blain S,, Laan P,, Sarthou G,, Veldhuis MJW,, Brussaard CPD,, Viollier E,, Timmermans KR. 2008. Fe-binding dissolved organic ligands near the Kerguelen Archipelago in the Southern Ocean (Indian sector). Deep-Sea Res 55( 5–7) : 606 621. doi: 10.1016/J.Dsr2.2007.12.007. http://dx.doi.org/10.1016/J.Dsr2.2007.12.007
125. Boukhalfa H,, Crumbliss AL. 2002. Chemical aspects of siderophore mediated iron transport. Biometals 15( 4) : 325 339.[PubMed][CrossRef]
126. Luu YS,, Ramsay JA. 2003. Review: microbial mechanisms of accessing insoluble Fe(III) as an energy source. World J Microb Biot 19( 2) : 215 225. doi: 10.1023/A:1023225521311.[CrossRef] http://dx.doi.org/10.1023/A:1023225521311
127. Finking R,, Marahiel MA. 2004. Biosynthesis of nonribosomal peptides 1. Ann Rev Microbiol 58 : 453 488. doi: 10.1146/annurev.micro.58.030603.123615.[CrossRef] http://dx.doi.org/10.1146/annurev.micro.58.030603.123615
128. Crosa JH,, Walsh CT. 2002. Genetics and assembly line enzymology of siderophore biosynthesis in bacteria. Microbiol Mol Biol Rev 66( 2) : 223 249.[PubMed][CrossRef]
129. Ledyard KM,, Butler A. 1997. Structure of putrebactin, a new dihydroxamate siderophore produced by Shewanella putrefaciens. J Biol Inorg Chem 2( 1) : 93 97. doi: 10.1007/S007750050110.[CrossRef] http://dx.doi.org/10.1007/S007750050110
130. Jones ME,, Fennessey CM,, DiChristina TJ,, Taillefert M. 2010. Shewanella oneidensis MR-1 mutants selected for their inability to produce soluble organic-Fe(III) complexes are unable to respire Fe(III) as anaerobic electron acceptor. Environ Microbiol 12( 4) : 938 950. doi: 10.1111/j.1462–2920.2009.02137.x.[PubMed][CrossRef] http://dx.doi.org/10.1111/j.1462–2920.2009.02137.x
131. Brendel PJ,, Luther GW. 1995. Development of a gold amalgam voltammetric microelectrode for the determination of dissolved Fe, Mn, O 2, and S(-II) in porewaters of marine and freshwater sediments. Environ Sci Technol 29( 3) : 751 761. doi: 10.1021/es00003a024.[PubMed][CrossRef] http://dx.doi.org/10.1021/es00003a024
132. Taillefert M,, Bono AB,, Luther GW. 2000. Reactivity of freshly formed Fe(III) in synthetic solutions and (pore)waters: voltammetric evidence of an aging process. Environ Sci Technol 34( 11) : 2169 2177. doi: 10.1021/Es990120a.[CrossRef] http://dx.doi.org/10.1021/Es990120a
133. Taillefert M,, Hover VC,, Rozan TF,, Theberge SM,, Luther GW. 2002. The influence of sulfides on soluble organic-Fe(III) in anoxic sediment porewaters. Estuaries 25( 6A): 1088 1096. doi: 10.1007/Bf02692206.[CrossRef] http://dx.doi.org/10.1007/Bf02692206
134. Arnold RG,, DiChristina TJ,, Hoffmann MR. 1986. Inhibitor studies of dissimilative Fe(III) reduction by Pseudomonas sp. strain 200 (“ Pseudomonas ferrireductans”). Appl Environ Microbiol 52( 2) : 281 289.[PubMed]
135. Myers CR,, Myers JM. 2003. Cell surface exposure of the outer membrane cytochromes of Shewanella oneidensis MR-1. Lett Appl Microbiol 37( 3) : 254 258. doi: 10.1046/J.1472–765x.2003.01389.X.[PubMed][CrossRef] http://dx.doi.org/10.1046/J.1472–765x.2003.01389.X
136. Nevin KP,, Lovley DR. 2002. Mechanisms for accessing insoluble Fe(III) oxide during dissimilatory Fe(III) reduction by Geothrix fermentans. Appl Environ Microbiol 68( 5) : 2294 2299. doi: 10.1128/Aem.68.5.2294-2299.2002.[PubMed][CrossRef] http://dx.doi.org/10.1128/Aem.68.5.2294-2299.2002
137. Haas JR,, DiChristina TJ. 2002. Effects of Fe(III) chemical speciation on dissimilatory Fe(III) reduction by Shewanella putrefaciens. Environ Sci Technol 36( 3) : 373 380.[PubMed][CrossRef]

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error