Skip to main content

The Biochemistry of Dissimilatory Ferric Iron and Manganese Reduction in Shewanella oneidensis

  • Chapter
  • First Online:

Abstract

More than two decades ago, Kenneth Nealson and Charles Myers published a seminal manuscript, describing an organism that can couple growth to the respiratory reduction of manganese oxide, an extracellular electron acceptor. This was the starting point of research aiming to elucidate mechanisms of extracellular respiration in a γ-proteobacterium named Shewanella oneidensis. This research is manifested in a nearly confusing multitude of publications that are sometimes even contradictory. It is the aim of this chapter to give a thorough overview of our knowledge about the biochemistry of metal respiration in S. oneidensis. This chapter starts off with a technological survey describing the molecular toolbox we have in our hands to genetically modify S. oneidensis. Thereafter, the path of electrons from the cytoplasmic membrane to the cell surface is followed, and thereby potential proteins for this electron transport and the transfer onto terminal metallic electron acceptors are brought to the reader’s attention. Moreover, the potential role of further proteins is analyzed that are not necessarily involved in the electron transport chain to ferric iron or manganese oxides per se but still seem to provide a selective advantage for the organism. Throughout the text it will become clear that the list of open questions concerning S. oneidensis physiology is still, even after decades of research and although it is the best studied dissimilatory metal reducer, extensive, and that there is room for more fascinating questions that can be addressed using the system S. oneidensis.

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Atack JM, Kelly DJ (2007) Structure, mechanism and physiological roles of bacterial cytochrome c peroxidases. Adv Microb Physiol 52:73–106

    Article  PubMed  CAS  Google Scholar 

  • Atkinson SJ, Mowat CG, Reid GA, Chapman SK (2007) An octaheme c-type cytochrome from Shewanella oneidensis can reduce nitrite and hydroxylamine. FEBS Lett 581:3805–3808

    Article  PubMed  CAS  Google Scholar 

  • Beliaev AS, Saffarini DA (1998) Shewanella putrefaciens mtrB encodes an outer membrane protein required for Fe(III) and Mn(IV) reduction. J Bacteriol 180:6292–6297

    PubMed  CAS  Google Scholar 

  • Beliaev AS, Thompson DK, Khare T, Lim H, Brandt CC, Li G, Murray AE, Heidelberg JF, Giometti CS, Yates J 3rd, Nealson KH, Tiedje JM, Zhoui J (2002) Gene and protein expression profiles of Shewanella oneidensis during anaerobic growth with different electron acceptors. OMICS 6:39–60

    Article  PubMed  CAS  Google Scholar 

  • Beliaev AS, Klingeman DM, Klappenbach JA, Wu L, Romine MF, Tiedje JM, Nealson KH, Fredrickson JK, Zhou J (2005) Global transcriptome analysis of Shewanella oneidensis MR-1 exposed to different terminal electron acceptors. J Bacteriol 187:7138–7145

    Article  PubMed  CAS  Google Scholar 

  • Blattner FR, Plunkett G 3rd, Bloch CA, Perna NT, Burland V, Riley M, Collado-Vides J, Glasner JD, Rode CK, Mayhew GF, Gregor J, Davis NW, Kirkpatrick HA, Goeden MA, Rose DJ, Mau B, Shao Y (1997) The complete genome sequence of Escherichia coli K-12. Science 277:1453–1462

    Article  PubMed  CAS  Google Scholar 

  • Bos MP, Robert V, Tommassen J (2007) Biogenesis of the gram-negative bacterial outer membrane. Annu Rev Microbiol 61:191–214

    Article  PubMed  CAS  Google Scholar 

  • Bouhenni R, Gehrke A, Saffarini D (2005) Identification of genes involved in cytochrome c biogenesis in Shewanella oneidensis, using a modified mariner transposon. Appl Environ Microbiol 71:4935–4937

    Article  PubMed  CAS  Google Scholar 

  • 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. Electroanal 22:856–864

    Article  CAS  Google Scholar 

  • Braun V, Hantke K (2011) Recent insights into iron import by bacteria. Curr Opin Chem Biol 15:328–334

    Article  PubMed  CAS  Google Scholar 

  • Bretschger O, Obraztsova A, Sturm CA, Chang IS, Gorby YA, Reed SB, Culley DE, Reardon CL, Barua S, Romine MF, Zhou J, Beliaev AS, Bouhenni R, Saffarini D, Mansfeld F, Kim BH, Fredrickson JK, Nealson KH (2007) Current production and metal oxide reduction by Shewanella oneidensis MR-1 wild type and mutants. Appl Environ Microbiol 73:7003–7012

    Article  PubMed  CAS  Google Scholar 

  • Brown RN, Romine MF, Schepmoes AA, Smith RD, Lipton MS (2010) Mapping the subcellular proteome of Shewanella oneidensis MR-1 using sarkosyl-based fractionation and LC-MS/MS protein identification. J Proteome Res 9:4454–4463

    Article  PubMed  CAS  Google Scholar 

  • Bücking C, Popp F, Kerzenmacher S, Gescher J (2010) Involvement and specificity of Shewanella oneidensis outer membrane cytochromes in the reduction of soluble and solid-phase terminal electron acceptors. FEMS Microbiol Lett 306:144–151

    Article  PubMed  CAS  Google Scholar 

  • Bücking C, Piepenbrock A, Kappler A, Gescher J (2012) Outer membrane cytochrome independent reduction of extracellular electron acceptors in Shewanella oneidensis. Microbiology (Epub ahead of print)

    Google Scholar 

  • Burns JL, DiChristina TJ (2009) Anaerobic respiration of elemental sulfur and thiosulfate by Shewanella oneidensis MR-1 requires psrA, a homolog of the phsA gene of Salmonella enterica serovar typhimurium LT2. Appl Environ Microbiol 75:5209–5217

    Article  PubMed  CAS  Google Scholar 

  • Cabiscol E, Piulats E, Echave P, Herrero E, Ros J (2000) Oxidative stress promotes specific protein damage in Saccharomyces cerevisiae. J Biol Chem 275:27393–27398

    PubMed  CAS  Google Scholar 

  • Carpentier W, De Smet L, Van Beeumen J, Brige A (2005) Respiration and growth of Shewanella oneidensis MR-1 using vanadate as the sole electron acceptor. J Bacteriol 187:3293–3301

    Article  PubMed  CAS  Google Scholar 

  • 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 U S A 108:9384–9389

    Article  PubMed  CAS  Google Scholar 

  • Coursolle D, Gralnick JA (2010) Modularity of the Mtr respiratory pathway of Shewanella oneidensis strain MR-1. Mol Microbiol

    Google Scholar 

  • Cruz-Garcia C, Murray AE, Klappenbach JA, Stewart V, Tiedje JM (2007) Respiratory nitrate ammonification by Shewanella oneidensis MR-1. J Bacteriol 189:656–662

    Article  PubMed  CAS  Google Scholar 

  • 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 184:142–151

    Article  PubMed  CAS  Google Scholar 

  • Dobbin PS, Butt JN, Powell AK, Reid GA, Richardson DJ (1999) Characterization of a flavocytochrome that is induced during the anaerobic respiration of Fe3+ by Shewanella frigidimarina NCIMB400. Biochem J 342(Pt 2):439–448

    Article  PubMed  CAS  Google Scholar 

  • 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 U S A 107:18127–18131

    Article  PubMed  CAS  Google Scholar 

  • Elias DA, Monroe ME, Marshall MJ, Romine MF, Belieav AS, Fredrickson JK, Anderson GA, Smith RD, Lipton MS (2005) Global detection and characterization of hypothetical proteins in Shewanella oneidensis MR-1 using LC-MS based proteomics. Proteomics 5:3120–3130

    Article  PubMed  CAS  Google Scholar 

  • Elias DA, Monroe ME, Smith RD, Fredrickson JK, Lipton MS (2006) Confirmation of the expression of a large set of conserved hypothetical proteins in Shewanella oneidensis MR-1. J Microbiol Methods 66:223–233

    Article  PubMed  CAS  Google Scholar 

  • Elias DA, Yang F, Mottaz HM, Beliaev AS, Lipton MS (2007) Enrichment of functional redox reactive proteins and identification by mass spectrometry results in several terminal Fe(III)-reducing candidate proteins in Shewanella oneidensis MR-1. J Microbiol Methods 68:367–375

    Article  PubMed  CAS  Google Scholar 

  • Esteve-Nunez A, Sosnik J, Visconti P, Lovley DR (2008) Fluorescent properties of c-type cytochromes reveal their potential role as an extracytoplasmic electron sink in Geobacter sulfurreducens. Environ Microbiol 10:497–505

    Article  PubMed  CAS  Google Scholar 

  • Firer-Sherwood M, Pulcu GS, Elliott SJ (2008) Electrochemical interrogations of the Mtr cytochromes from Shewanella: opening a potential window. J Biol Inorg Chem 13:849–854

    Article  PubMed  CAS  Google Scholar 

  • Fonseca BM, Saraiva IH, Paquete CM, Soares CM, Pacheco I, Salgueiro CA, Louro RO (2009) The tetraheme cytochrome from Shewanella oneidensis MR-1 shows thermodynamic bias for functional specificity of the hemes. J Biol Inorg Chem 14:375–385

    Article  PubMed  CAS  Google Scholar 

  • Gao H, Yang ZK, Barua S, Reed SB, Romine MF, Nealson KH, Fredrickson JK, Tiedje JM, Zhou J (2009) Reduction of nitrate in Shewanella oneidensis depends on atypical NAP and NRF systems with NapB as a preferred electron transport protein from CymA to NapA. ISME J 3:966–976

    Article  PubMed  CAS  Google Scholar 

  • 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. Microbiol Biotechnol 3:455–466

    Article  CAS  Google Scholar 

  • 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 68:706–719

    Article  PubMed  CAS  Google Scholar 

  • Gorby Y, McLean J, Korenevsky A, Rosso K, El-Naggar MY, Beveridge TJ (2008) Redox-reactive membrane vesicles produced by Shewanella. Geobiology 6:232–241

    Article  PubMed  CAS  Google Scholar 

  • 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 103:11358–11363

    Article  PubMed  CAS  Google Scholar 

  • Gralnick JA, Vali H, Lies DP, Newman DK (2006) Extracellular respiration of dimethyl sulfoxide by Shewanella oneidensis strain MR-1. Proc Natl Acad Sci U S A 103:4669–4674

    Article  PubMed  CAS  Google Scholar 

  • Gunsalus RP (1992) Control of electron flow in Escherichia coli: coordinated transcription of respiratory pathway genes. J Bacteriol 174:7069–7074

    PubMed  CAS  Google Scholar 

  • 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 12:1083–1094

    Article  PubMed  CAS  Google Scholar 

  • 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 U S A 106:22169–22174

    Article  PubMed  CAS  Google Scholar 

  • Hunt KA, Flynn JM, Naranjo B, Shikhare ID, Gralnick JA (2010) Substrate-level phosphorylation is the primary source of energy conservation during anaerobic respiration of Shewanella oneidensis strain MR-1. J Bacteriol 192:3345–3351

    Article  PubMed  CAS  Google Scholar 

  • Jiao Y, Newman DK (2007) The pio operon is essential for phototrophic Fe(II) oxidation in Rhodopseudomonas palustris TIE-1. J Bacteriol 189:1765–1773

    Article  PubMed  CAS  Google Scholar 

  • 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 12:938–950

    Article  PubMed  CAS  Google Scholar 

  • Karpinets TV, Romine MF, Schmoyer DD, Kora GH, Syed MH, Leuze MR, Serres MH, Park BH, Samatova NF, Uberbacher EC (2010) Shewanella knowledgebase: integration of the experimental data and computational predictions suggests a biological role for transcription of intergenic regions. Database (Oxford) 2010. baq012

    Google Scholar 

  • Kerisit S, Rosso KM (2007) Kinetic Monte Carlo model of charge transport in hematite (alpha-Fe(2)O(3)). J Chem Phys 127:124706

    Article  PubMed  CAS  Google Scholar 

  • Kolker E, Picone AF, Galperin MY, Romine MF, Higdon R, Makarova KS, Kolker N, Anderson GA, Qiu X, Auberry KJ, Babnigg G, Beliaev AS, Edlefsen P, Elias DA, Gorby YA, Holzman T, Klappenbach JA, Konstantinidis KT, Land ML, Lipton MS, McCue LA, Monroe M, Pasa-Tolic L, Pinchuk G, Purvine S, Serres MH, Tsapin S, Zakrajsek BA, Zhu W, Zhou J, Larimer FW, Lawrence CE, Riley M, Collart FR, Yates JR 3rd, Smith RD, Giometti CS, Nealson KH, Fredrickson JK, Tiedje JM (2005) Global profiling of Shewanella oneidensis MR-1: expression of hypothetical genes and improved functional annotations. Proc Natl Acad Sci U S A 102:2099–2104

    Article  PubMed  CAS  Google Scholar 

  • Kulp A, Kuehn MJ (2010) Biological functions and biogenesis of secreted bacterial outer membrane vesicles. Annu Rev Microbiol 64:163–184

    Article  PubMed  CAS  Google Scholar 

  • Learman DR, Yi H, Brown SD, Martin SL, Geesey GG, Stevens AM, Hochella MF Jr (2009) Involvement of Shewanella oneidensis MR-1 LuxS in biofilm development and sulfur metabolism. Appl Environ Microbiol 75:1301–1307

    Article  PubMed  CAS  Google Scholar 

  • Leys D, Tsapin AS, Nealson KH, Meyer TE, Cusanovich MA, Van Beeumen JJ (1999) Structure and mechanism of the flavocytochrome c fumarate reductase of Shewanella putrefaciens MR-1. Nat Struct Biol 6:1113–1117

    Article  PubMed  CAS  Google Scholar 

  • 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 277:35703–35711

    Article  PubMed  CAS  Google Scholar 

  • 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 71:4414–4426

    Article  PubMed  CAS  Google Scholar 

  • Liu J, Wang Z, Belchik SM, Edwards MJ, Liu C, Kennedy DW, Merkley ED, Lipton MS, Butt JN, Richardson DJ, Zachara JM, Fredrickson JK, Rosso KM, Shi L (2012) Identification and characterization of MtoA: a decaheme c-type cytochrome of the neutrophilic Fe(II)-oxidizing bacterium Sideroxydans lithotrophicus ES-1. Front Microbiol 3:37

    PubMed  CAS  Google Scholar 

  • Lomize AL, Pogozheva ID, Lomize MA, Mosberg HI (2006) Positioning of proteins in membranes: a computational approach. Protein Sci 15:1318–1333

    Article  PubMed  CAS  Google Scholar 

  • Lower BH, Lins RD, Oestreicher Z, Straatsma TP, Hochella MF Jr, Shi L, Lower SK (2008) In vitro evolution of a peptide with a hematite binding motif that may constitute a natural metal-oxide binding archetype. Environ Sci Technol 42:3821–3827

    Article  PubMed  CAS  Google Scholar 

  • 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:e268

    Article  PubMed  CAS  Google Scholar 

  • 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 U S A 105:3968–3973

    Article  PubMed  CAS  Google Scholar 

  • McLean JS, Pinchuk GE, Geydebrekht OV, Bilskis CL, Zakrajsek BA, Hill EA, Saffarini DA, Romine MF, Gorby YA, Fredrickson JK, Beliaev AS (2008) Oxygen-dependent autoaggregation in Shewanella oneidensis MR-1. Environ Microbiol 10:1861–1876

    Article  PubMed  CAS  Google Scholar 

  • McMillan DG, Marritt SJ, Butt JN, Jeuken LJ (2012) Menaquinone-7 is specific cofactor in tetraheme quinol dehydrogenase CymA. J Biol Chem 287:14215–14225

    Article  PubMed  CAS  Google Scholar 

  • Meyer TE, Tsapin AI, Vandenberghe I, de Smet L, Frishman D, Nealson KH, Cusanovich MA, van Beeumen JJ (2004) Identification of 42 possible cytochrome c genes in the Shewanella oneidensis genome and characterization of six soluble cytochromes. OMICS 8:57–77

    Article  PubMed  CAS  Google Scholar 

  • Morris CJ, Black AC, Pealing SL, Manson FD, Chapman SK, Reid GA, Gibson DM, Ward FB (1994) Purification and properties of a novel cytochrome: flavocytochrome c from Shewanella putrefaciens. Biochem J 302(Pt 2):587–593

    PubMed  CAS  Google Scholar 

  • Mowat CG, Rothery E, Miles CS, McIver L, Doherty MK, Drewette K, Taylor P, Walkinshaw MD, Chapman SK, Reid GA (2004) Octaheme tetrathionate reductase is a respiratory enzyme with novel heme ligation. Nat Struct Mol Biol 11:1023–1024

    Article  PubMed  CAS  Google Scholar 

  • Murphy JN, Saltikov CW (2007) The cymA gene, encoding a tetraheme c-type cytochrome, is required for arsenate respiration in Shewanella species. J Bacteriol 189:2283–2290

    Article  PubMed  CAS  Google Scholar 

  • Myers CR, Nealson KH (1988) Bacterial manganese reduction and growth with manganese oxide as the sole electron-acceptor. Science 240:1319–1321

    Article  PubMed  CAS  Google Scholar 

  • Myers CR, Myers JM (1997a) Isolation and characterization of a transposon mutant of Shewanella putrefaciens MR-1 deficient in fumarate reductase. Lett Appl Microbiol 25:162–168

    Article  PubMed  CAS  Google Scholar 

  • Myers CR, Myers JM (1997b) 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 179:1143–1152

    PubMed  CAS  Google Scholar 

  • Myers CR, Myers JM (1997c) Replication of plasmids with the p15A origin in Shewanella putrefaciens MR-1. Lett Appl Microbiol 24:221–225

    Article  PubMed  CAS  Google Scholar 

  • Myers CR, Myers JM (2002a) MtrB is required for proper incorporation of the cytochromes OmcA and OmcB into the outer membrane of Shewanella putrefaciens MR-1. Appl Environ Microbiol 68:5585–5594

    Article  PubMed  CAS  Google Scholar 

  • Myers CR, Myers JM (2003a) Cell surface exposure of the outer membrane cytochromes of Shewanella oneidensis MR-1. Lett Appl Microbiol 37:254–258

    Article  PubMed  CAS  Google Scholar 

  • Myers CR, Myers JM (2004a) The outer membrane cytochromes of Shewanella oneidensis MR-1 are lipoproteins. Lett Appl Microbiol 39:466–470

    Article  PubMed  CAS  Google Scholar 

  • Myers CR, Myers JM (2004b) Shewanella oneidensis MR-1 restores menaquinone synthesis to a menaquinone-negative mutant. Appl Environ Microbiol 70:5415–5425

    Article  PubMed  CAS  Google Scholar 

  • 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 67:260–269

    Article  PubMed  CAS  Google Scholar 

  • Myers JM, Myers CR (2002b) Genetic complementation of an outer membrane cytochrome omcB mutant of Shewanella putrefaciens MR-1 requires omcB plus downstream DNA. Appl Environ Microbiol 68:2781–2793

    Article  PubMed  CAS  Google Scholar 

  • Myers JM, Myers CR (2003b) Overlapping role of the outer membrane cytochromes of Shewanella oneidensis MR-1 in the reduction of manganese(IV) oxide. Lett Appl Microbiol 37:21–25

    Article  PubMed  CAS  Google Scholar 

  • Newman DK, Kolter R (2000) A role for excreted quinones in extracellular electron transfer. Nature 405:94–97

    Article  PubMed  CAS  Google Scholar 

  • Paquete CM, Saraiva IH, Calcada E, Louro RO (2010) Molecular basis for directional electron transfer. J Biol Chem 285:10370–10375

    Article  PubMed  CAS  Google Scholar 

  • Pauleta SR, Cooper A, Nutley M, Errington N, Harding S, Guerlesquin F, Goodhew CF, Moura I, Moura JJG, Pettigrew GW (2004) A copper protein and a cytochrome bind at the same site on bacterial cytochrome c peroxidase. Biochemistry 43:14566–14576

    Article  PubMed  CAS  Google Scholar 

  • Pessanha M, Rothery EL, Miles CS, Reid GA, Chapman SK, Louro RO, Turner DL, Salgueiro CA, Xavier AV (2009) Tuning of functional heme reduction potentials in Shewanella fumarate reductases. Biochim Biophys Acta 1787:113–120

    Article  PubMed  CAS  Google Scholar 

  • 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 278:27758–27765

    Article  PubMed  CAS  Google Scholar 

  • Qian Y, Paquete CM, Louro RO, Ross DE, Labelle E, Bond DR, Tien M (2011a) Mapping the iron binding site(s) on the small tetraheme cytochrome of Shewanella oneidensis MR-1. Biochemistry 50:6217–6224

    Article  PubMed  CAS  Google Scholar 

  • Qian Y, Shi L, Tien M (2011b) SO2907, A putative TonB-dependent receptor, is involved in dissimilatory iron reduction by Shewanella oneidensis MR-1. J Biol Chem 286:33973–33980

    Article  PubMed  CAS  Google Scholar 

  • 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 8:56–68

    Article  PubMed  CAS  Google Scholar 

  • Reguera G, McCarthy KD, Mehta T, Nicoll JS, Tuominen MT, Lovley DR (2005) Extracellular electron transfer via microbial nanowires. Nature 435:1098–1101

    Article  PubMed  CAS  Google Scholar 

  • Richter K, Bücking C, Schicklberger M, Gescher J (2010) A simple and fast method to analyze the orientation of c-type cytochromes in the outer membrane of Gram-negative bacteria. J Microbiol Methods 82:184–186

    Article  PubMed  CAS  Google Scholar 

  • Rodrigues ML, Oliveira TF, Pereira IA, Archer M (2006) X-ray structure of the membrane-bound cytochrome c quinol dehydrogenase NrfH reveals novel haem coordination. EMBO J 25:5951–5960

    Article  PubMed  CAS  Google Scholar 

  • Romine MF, Carlson TS, Norbeck AD, McCue LA, Lipton MS (2008) Identification of mobile elements and pseudogenes in the Shewanella oneidensis MR-1 genome. Appl Environ Microbiol 74:3257–3265

    Article  PubMed  CAS  Google Scholar 

  • 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 73:5797–5808

    Article  PubMed  CAS  Google Scholar 

  • Ross DE, Brantley SL, Tien M (2009) Kinetic characterization of terminal reductases OmcA and MtrC involved in respiratory electron transfer for dissimilatory iron reduction in Shewanella oneidensis MR-1. Appl Environ Microbiol 75:5218–5226

    Article  PubMed  CAS  Google Scholar 

  • Saffarini DA, Blumerman SL, Mansoorabadi KJ (2002) Role of menaquinones in Fe(III) reduction by membrane fractions of Shewanella putrefaciens. J Bacteriol 184:846–848

    Article  PubMed  CAS  Google Scholar 

  • Saltikov CW, Newman DK (2003) Genetic identification of a respiratory arsenate reductase. Proc Natl Acad Sci U S A 100:10983–10988

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T, Russell DW (1989) Molecular cloning. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Schicklberger M, Bücking C, Schuetz B, Heide H, Gescher J (2010) Involvement of the Shewanella oneidensis decaheme cytochrome MtrA in the periplasmic stability of the beta-barrel protein MtrB. Appl Environ Microbiol 77:1520–1523

    Article  PubMed  CAS  Google Scholar 

  • 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 75:7789–7796. doi:10.1128/AEM.01834-09

    Article  PubMed  CAS  Google Scholar 

  • Schütz B, Seidel J, Sturm G, Einsle O, Gescher J (2011) Investigation of the electron transport chain to and the catalytic activity of the diheme cytochrome c peroxidase CcpA of Shewanella oneidensis. Appl Environ Microbiol 77:6172–6180. doi:10.1128/AEM.00606-11

    Article  PubMed  CAS  Google Scholar 

  • 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 30:658–662

    Article  PubMed  CAS  Google Scholar 

  • 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 42:9491–9497

    Article  PubMed  CAS  Google Scholar 

  • Scott JH, Nealson KH (1994) A biochemical study of the intermediary carbon metabolism of Shewanella putrefaciens. J Bacteriol 176:3408–3411

    PubMed  CAS  Google Scholar 

  • Shanks RM, Caiazza NC, Hinsa SM, Toutain CM, O’Toole GA (2006) Saccharomyces cerevisiae-based molecular tool kit for manipulation of genes from gram-negative bacteria. Appl Environ Microbiol 72:5027–5036

    Article  PubMed  CAS  Google Scholar 

  • 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 188:4705–4714

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Shirodkar S, Reed S, Romine M, Saffarini D (2011) The octahaem SirA catalyses dissimilatory sulfite reduction in Shewanella oneidensis MR-1. Environ Microbiol 13:108–115

    Article  PubMed  CAS  Google Scholar 

  • Shyu JB, Lies DP, Newman DK (2002) Protective role of tolC in efflux of the electron shuttle anthraquinone-2,6-disulfonate. J Bacteriol 184:1806–1810

    Article  PubMed  CAS  Google Scholar 

  • Sklar JG, Wu T, Kahne D, Silhavy TJ (2007) Defining the roles of the periplasmic chaperones SurA, Skp, and DegP in Escherichia coli. Genes Dev 21:2473–2484

    Article  PubMed  CAS  Google Scholar 

  • Spiess C, Beil A, Ehrmann M (1999) A temperature-dependent switch from chaperone to protease in a widely conserved heat shock protein. Cell 97:339–347

    Article  PubMed  CAS  Google Scholar 

  • Sturm G, Gescher J About the periplasmic electron transfer network in S. oneidensis (In preparation)

    Google Scholar 

  • Thauer RK, Jungermann K, Decker K (1977) Energy conservation in chemotrophic anaerobic bacteria. Bacteriol Rev 41:100–180

    PubMed  CAS  Google Scholar 

  • Thormann KM, Saville RM, Shukla S, Pelletier DA, Spormann AM (2004) Initial phases of biofilm formation in Shewanella oneidensis MR-1. J Bacteriol 186:8096–8104

    Article  PubMed  CAS  Google Scholar 

  • Thormann KM, Saville RM, Shukla S, Spormann AM (2005) Induction of rapid detachment in Shewanella oneidensis MR-1 biofilms. J Bacteriol 187:1014–1021

    Article  PubMed  CAS  Google Scholar 

  • Unden G, Bongaerts J (1997) Alternative respiratory pathways of Escherichia coli: energetics and transcriptional regulation in response to electron acceptors. Biochim Biophys Acta 1320:217–234

    Article  PubMed  CAS  Google Scholar 

  • Uria N, Munoz Berbel X, Sanchez O, Munoz FX, Mas J (2011) Transient storage of electrical charge in biofilms of Shewanella oneidensis MR-1 growing in a microbial fuel cell. Environ Sci Technol 45(23):10250–10256

    Google Scholar 

  • Venkateswaran K, Moser DP, Dollhopf ME, Lies DP, Saffarini DA, MacGregor BJ, Ringelberg DB, White DC, Nishijima M, Sano H, Burghardt J, Stackebrandt E, Nealson KH (1999) Polyphasic taxonomy of the genus Shewanella and description of Shewanella oneidensis sp. nov. Int J Syst Bacteriol 49 Pt 2:705–724

    Google Scholar 

  • 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 74:615–623

    Article  CAS  Google Scholar 

  • Yang C, Rodionov DA, Li X, Laikova ON, Gelfand MS, Zagnitko OP, Romine MF, Obraztsova AY, Nealson KH, Osterman AL (2006) Comparative genomics and experimental characterization of N-acetylglucosamine utilization pathway of Shewanella oneidensis. J Biol Chem 281:29872–29885

    Article  PubMed  CAS  Google Scholar 

  • Zhang H, Yang F, Qian WJ, Brown RN, Wang Y, Merkley EE, Park JH, Monroe ME, Purvine SO, Moore RJ, Shi L, Fredrickson JK, Pasa-Tolic L, Smith RD, Lipton MS (2011) Identification of c-type heme-containing peptides using nonactivated immobilized metal affinity chromatography resin enrichment and higher-energy collisional dissociation. Anal Chem 83:7260–7268

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Johannes Gescher .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Bücking, C., Schicklberger, M., Gescher, J. (2013). The Biochemistry of Dissimilatory Ferric Iron and Manganese Reduction in Shewanella oneidensis . In: Gescher, J., Kappler, A. (eds) Microbial Metal Respiration. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-32867-1_3

Download citation

Publish with us

Policies and ethics