Reduction of low potential electron acceptors requires the CbcL inner membrane cytochrome of Geobacter sulfurreducens

Bioelectrochemistry

Volumn 107, Issue , 2016, Pages 7-13

  Zacharoff, Lori ^a   Chan, Chi Ho ^a   Bond, Daniel R ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Cytochrome; Extracellular respiration; Geobacter; Metal reduction; Microbial electrochemical cell

Indexed keywords

ELECTRODES; ELECTRON TRANSITIONS; MEMBRANES; PROTEINS; REDOX REACTIONS; REDUCTION;

C-TYPE CYTOCHROME; ELECTRON ACCEPTOR; ELECTRON TRANSFER; EXTRACELLULAR; GEOBACTER; GEOBACTER SULFURREDUCENS; METAL REDUCTION; REDOX POTENTIALS;

CYCLIC VOLTAMMETRY;

CBCL PROTEIN; CYTOCHROME; FERRIC OXIDE; HEME; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; FERRIC CITRATE; FERRIC ION; MANGANESE DERIVATIVE; MANGANESE OXIDE; MEMBRANE PROTEIN; OXIDE;

ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL STRAIN; BIOFILM; CBCL GENE; CELL MEMBRANE; CONTROLLED STUDY; CYCLIC POTENTIOMETRY; ELECTROCHEMICAL ANALYSIS; ELECTRON TRANSPORT; GENE DELETION; GENE EXPRESSION; GEOBACTER SULFURREDUCENS; INNER MEMBRANE; NONHUMAN; OXIDATION REDUCTION POTENTIAL; BIOENERGY; ELECTROCHEMISTRY; ELECTRODE; ENZYMOLOGY; GENETICS; GEOBACTER; GROWTH, DEVELOPMENT AND AGING; METABOLISM;

BACTERIAL PROTEINS; BIOELECTRIC ENERGY SOURCES; BIOFILMS; CYTOCHROMES; ELECTROCHEMISTRY; ELECTRODES; ELECTRON TRANSPORT; FERRIC COMPOUNDS; GENE DELETION; GEOBACTER; MANGANESE COMPOUNDS; MEMBRANE PROTEINS; OXIDES;

EID: 84942540560     PISSN: 15675394     EISSN: 1878562X     Source Type: Journal    
DOI: 10.1016/j.bioelechem.2015.08.003     Document Type: Article

References (34)

1. Weber K.A., Urrutia M.M., Churchill P.F., Kukkadapu R.K., Roden E.E. Anaerobic redox cycling of iron by freshwater sediment microorganisms. Environ. Microbiol. 2005, 8:100-113.
2. Blöthe M., Roden E.E. Microbial iron redox cycling in a circumneutral-pH groundwater seep. Appl. Environ. Microbiol. 2009, 75:468-473.
3. Simon J., van Spanning R.J.M., Richardson D.J. The organisation of proton motive and non-proton motive redox loops in prokaryotic respiratory systems. Biochim. Biophys. Acta 2008, 1777:1480-1490.
4. Salas E.C., Berelson W.M., Hammond D.E., Kampf A.R., Nealson K.H. The impact of bacterial strain on the products of dissimilatory iron reduction. Geochim. Cosmochim. Acta 2011, 74:574-583.
5. Majzlan J. Minerals and aqueous species of iron and manganese as reactants and products of microbial metal respiration. Microb. Met. Respir. from Geochemistry to Potential Applications 2012, 112-128. Springer Verlag, New York, NY. 1st ed. J. Gescher, A. Kappler (Eds.).
6. Zhu X., Yates M.D., Hatzell M.C., Rao H.A., Saikaly P.E., Logan B.E. Microbial community composition is unaffected by anode potential. Environ. Sci. Technol. 2014, 1352-1358.
7. Commault A.S., Lear G., Packer M.A., Weld R.J. Influence of anode potentials on selection of Geobacter strains in microbial electrolysis cells. Bioresour. Technol. 2013, 139:226-234.
8. Ishii S., Suzuki S., Norden-Krichmar T.M., Tenney A., Chain P.S.G., Scholz M.B., Nealson K., Bretschger O. A novel metatranscriptomic approach to identify gene expression dynamics during extracellular electron transfer. Nat. Commun. 1841, 4:1601.
9. Rimboud M., Desmond-Le Quemener E., Erable B., Bouchez T., Bergel A. Multi-system Nernst-Michaelis-Menten model applied to bioanodes formed from sewage sludge. Bioresour. Technol. 2015, 195:192-169.
10. Strycharz S.M., Malanoski A.P., Snider R.M., Yi H., Lovley D.R., Tender L.M. Application of cyclic voltammetry to investigate enhanced catalytic current generation by biofilm-modified anodes of Geobacter sulfurreducens strain DL1 vs. variant strain KN400. Energy Environ. Sci. 2011, 4:896-913.
11. Richter H., Nevin K.P., Jia H., Lowy D.A., Lovley D.R., Tender L.M. Cyclic voltammetry of biofilms of wild type and mutant Geobacter sulfurreducens on fuel cell anodes indicates possible roles of OmcB, OmcZ, type IV pili, and protons in extracellular electron transfer. Energy Environ. Sci. 2009, 2:506-516.
12. Yoho R.A., Popat S.C., Torres C.I. Dynamic potential-dependent electron transport pathway shifts in anode biofilms of Geobacter sulfurreducens. ChemSusChem 2014, 3413-3419.
13. Levar C.E., Chan C.H., Mehta-kolte M.G., Bond D.R. An inner membrane cytochrome required only for reduction of high redox potential extracellular electron acceptors. MBio 2014, 5(6):1-9.
14. Butler J.E., Young N.D., Lovley D.R. Evolution of electron transfer out of the cell: comparative genomics of six Geobacter genomes. BMC Genomics 2010, 11:40.
15. Aklujkar M., Coppi M.V., Leang C., Kim B.C., Chavan M.A., Perpetua L.A., Giloteaux L., Liu A., Holmes D.E. Proteins involved in electron transfer to Fe(III) and Mn(IV) oxides by Geobacter sulfurreducens and Geobacter uraniireducens. Microbiology 2013, 159:515-535.
16. Ding Y.-H.R., Hixson K.K., Aklujkar M.A., Lipton M.S., Smith R.D., Lovley D.R., Mester T. Proteome of Geobacter sulfurreducens grown with Fe(III) oxide or Fe(III) citrate as the electron acceptor. Biochim. Biophys. Acta 2008, 1784:1935-1941.
17. Shrestha P.M., Rotaru A.-E., Aklujkar M., Liu F., Shrestha M., Summers Z.M., et al. Syntrophic growth with direct interspecies electron transfer as the primary mechanism for energy exchange. Environ. Microbiol. Rep. 2013, 5:904-910.
18. Ishii S., Suzuki S., Norden-Krichmar T.M., Phan T., Wanger G., Nealson K.H., Sekiguchi Y., Gorby Y., Bretschger O. Microbial population and functional dynamics associated with surface potential and carbon metabolism. ISME J. 2014, 8:963-978.
19. Marsili E., Rollefson J.B., Baron D.B., Hozalski R.M., Bond D.R. Microbial biofilm voltammetry: direct electrochemical characterization of catalytic electrode-attached biofilms. Appl. Environ. Microbiol. 2008, 74:7329-7337.
20. Lovley D.R., Phillips E.J.P. Organic matter mineralization with reduction of ferric Iron in anaerobic sediments organic matter mineralization with reduction of ferric iron in anaerobic sediments. Appl. Environ. Microbiol. 1986, 51:683-689.
21. Schafer A., Tauch A., Jager W., Kalinowski J., Thierbach G., Puhler A. Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutumicum. Gene 1994, 145:69-73.
22. Simon A., Priefer R., Puhler U. A broad host range mobilization system for in vivo genetic engineering: transposon mutagensis in gram negative bacteria. Biotechnology 1983, 1:784-791.
23. Fleige S., Pfaffl M.W. RNA integrity and the effect on the real-time qRT-PCR performance. Mol. Aspects Med. 2006, 27:126-139.
24. Jormakka M., Tornroth S., Byrne B., Iwata S. Molecular basis of proton motive force generation: structure of formate dehydrogenase-N. Science 2002, 295:1863-1868.
25. Qiu Y., Cho B.-K., Park Y.S., Lovley D., Palsson B.Ø., Zengler K. Structural and operational complexity of the Geobacter sulfurreducens genome. Genome Res. 2010, 20:1304-1311.
26. Straub K.L., Hanzlik M., Buchholz-Cleven B.E. The use of biologically produced ferrihydrite for the isolation of novel iron-reducing bacteria. Syst. Appl. Microbiol. 1998, 21:442-449.
27. Straub K.L., Schink B. Ferrihydrite reduction by Geobacter species is stimulated by secondary bacteria. Arch. Microbiol. 2004, 182:175-181.
28. Virdis B., Millo D., Donose B.C., Batstone D.J. Real-time measurements of the redox states of c-type cytochromes in electroactive biofilms: a confocal resonance raman microscopy study. PLoS One 2014, 9:e89918.
29. Virdis B., Harnisch F., Batstone D.J., Rabaey K., Donose B.C. Non-invasive characterization of electrochemically active microbial biofilms using confocal Raman microscopy. Energy Environ. Sci. 2012, 5:7017-7024.
30. Snider R.M., Strycharz-Glaven S.M., Tsoi S.D., Erickson J.S., Tender L.M. Long-range electron transport in Geobacter sulfurreducens biofilms is redox gradient-driven. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:15467-15472.
31. Torres C.I., Kato Marcus A., Rittmann B.E. Proton transport inside the biofilm limits electrical current generation by anode-respiring bacteria. Biotechnol. Bioeng. 2008, 100:872-881.
32. Hamelers H.V.M., Ter Heijne A., Stein N., Rozendal R.a., Buisman C.J.N. Butler-Volmer-Monod model for describing bio-anode polarization curves. Bioresour. Technol. 2011, 102:381-387.
33. Merkley E.D., Wrighton K., Castelle C.J., Anderson B.J., Wilkins M.J., Shah V., et al. Changes in protein expression across laboratory and field experiments in Geobacter bemidjiensis. J. Proteome Res. 2014, 1361-1375.
34. Rose N.D., Regan J.M. Changes in phosphorylation of adenosine phosphate and redox state of nicotinamide-adenine dinucleotide (phosphate) in Geobacter sulfurreducens in response to electron acceptor and anode potential variation. Bioelectrochemistry 2015, 106:213-220.