An inner membrane cytochrome required only for reduction of high redox potential extracellular electron acceptors

mBio

Volumn 5, Issue 6, 2014, Pages

  Levar, Caleb E ^a   Chan, Chi Ho ^a   Mehta Kolte, Misha G ^a   Bond, Daniel R ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMICAL COMPOUND; CYTOCHROME; CYTOCHROME C; EDETIC ACID; ELECTRON ACCEPTOR; FERRIC CITRATE; FERRIC ION; FERRIC OXIDE; HYDROGEN; MANGANESE OXIDE; UNCLASSIFIED DRUG; METAL;

ARTICLE; BACTERIAL GENE; BACTERIAL OUTER MEMBRANE; BIOENERGY; CONTROLLED STUDY; ELECTRODE; ELECTRON TRANSPORT; EXTRACELLULAR MATRIX; GENE DISRUPTION; GEOBACTER SULFURREDUCENS; GROWTH CURVE; IMCH GENE; INNER MEMBRANE; MICROBIAL ACTIVITY; MUTANT; NONHUMAN; OXIDATION REDUCTION POTENTIAL; RESPIRATORY SYSTEM; CELL MEMBRANE; ELECTRICITY; ENZYMOLOGY; GENE DELETION; GENETICS; GEOBACTER; GROWTH, DEVELOPMENT AND AGING; METABOLISM; OXIDATION REDUCTION REACTION;

GEOBACTER; GEOBACTER SULFURREDUCENS;

CELL MEMBRANE; CYTOCHROMES C; ELECTRICITY; GENE DELETION; GEOBACTER; METALS; OXIDATION-REDUCTION;

EID: 84920903442     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.02034-14     Document Type: Article

References (55)

1. Lovley DR, Holmes DE, Nevin KP. 2004. Dissimilatory Fe(III) and Mn(IV) reduction. Adv. Microb. Physiol. 49:219286. http://dx.doi.org/10.1016/S0065-2911(04)49005-5.
2. Caccavo F, Lonergan DJ, Lovley DR, Davis M, Stolz JF, McInerney MJ. 1994. Geobacter sulfurreducens sp. nov. a hydrogen-and acetate-oxidizing dissimilatory metal-reducing microorganism. Appl. Environ. Microbiol. 60:3752-3759.
3. Bond DR, Lovley DR. 2003. Electricity production by Geobacter sulfurreducens attached to electrodes. Appl. Environ. Microbiol. 69:1548-1555. http://dx.doi.org/10.1128/AEM.69.3.1548-1555.2003.
4. Snoeyenbos-West OL, Nevin KP, Anderson RT, Lovley DR. 2000. Enrichment of Geobacter species in response to stimulation of Fe(III) reduction in sandy aquifer sediments. Microb. Ecol. 39:153-167. http://dx.doi.org/10.1007/s002480000018.
5. Anderson RT, Vrionis HA, Ortiz-Bernad I, Resch CT, Long PE, Dayvault R, Karp K, Marutzky S, Metzler DR, Peacock A, White DC, Lowe M, Lovley DR. 2003. Stimulating the in situ activity of Geobacter species to remove uranium from the groundwater of a uranium-contaminated aquifer. Appl. Environ. Microbiol. 69:5884-5891. http://dx.doi.org/10.1128/AEM.69.10.5884-5891.2003.
6. Tadanier CJ, Schreiber ME, Roller JW. 2005. Arsenic mobilization through microbially mediated deflocculation of ferrihydrite. Environ. Sci. Technol. 39:3061-3068. http://dx.doi.org/10.1021/es048206d.
7. Islam FS, Gault AG, Boothman C, Polya DA, Charnock JM, Chatterjee D, Lloyd JR. 2004. Role of metal-reducing bacteria in arsenic release from Bengal delta sediments. Nature 430:68-71. http://dx.doi.org/10.1038/nature02638.
8. Bond DR, Holmes DE, Tender LM, Lovley DR. 2002. Electrodereducing microorganisms that harvest energy from marine sediments. Science 295:483-485. http://dx.doi.org/10.1126/science.1066771.
9. Holmes DE, Bond DR, O’Neil RA, Reimers CE, Tender LR, Lovley DR. 2004. Microbial communities associated with electrodes harvesting electricity from a variety of aquatic sediments. Microb. Ecol. 48:178-190. http://dx.doi.org/10.1007/s00248-003-0004-4.
10. Butler JE, Young ND, Lovley DR. 2010. Evolution of electron transfer out of the cell: comparative genomics of six Geobacter genomes. BMC Genomics 11:40. http://dx.doi.org/10.1186/1471-2164-11-40.
11. 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. 182:67-75. http://dx.doi.org/10.1128/JB.182.1.67-75.2000.
12. 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. 192:467-474. http://dx.doi.org/10.1128/JB.00925-09.
13. 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. http://dx.doi.org/10.1128/AEM.00146-07.
14. 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. http://dx.doi.org/10.1073/pnas.1017200108.
15. Saffarini DA, Schultz R, Beliaev A. 2003. Involvement of cyclic AMP (cAMP) and cAMP receptor protein in anaerobic respiration of Shewanella oneidensis. J. Bacteriol. 185:3668-3671. http://dx.doi.org/10.1128/JB.185.12.3668-3671.2003.
16. Nevin KP, Kim BC, Glaven RH, Johnson JP, Woodard TL, Methé BA, Didonato RJ, Covalla SF, Franks AE, Liu A, Lovley DR. 2009. Anode biofilm transcriptomics reveals outer surface components essential for high density current production in Geobacter sulfurreducens fuel cells. PLoS One 4:e5628. http://dx.doi.org/10.1371/journal.pone.0005628.
17. Ding YH, Hixson KK, Aklujkar MA, Lipton MS, Smith RD, Lovley DR, Mester T. 2008. Proteome of Geobacter sulfurreducens grown with Fe(III) oxide or Fe(III) citrate as the electron acceptor. Biochim. Biophys. Acta 1784:1935-1941. http://dx.doi.org/10.1016/j.bbapap.2008.06.011.
18. Ding YH, Hixson KK, Giometti CS, Stanley A, Esteve-Núñez A, Khare T, Tollaksen SL, Zhu W, Adkins JN, Lipton MS, Smith RD, Mester T, Lovley DR. 2006. The proteome of dissimilatory metal-reducing microorganism Geobacter sulfurreducens under various growth conditions. Biochim. Biophys. Acta 1764:1198-1206. http://dx.doi.org/10.1016/j.bbapap.2006.04.017.
19. Holmes DE, Chaudhuri SK, Nevin KP, Mehta T, Methé BA, Liu A, Ward JE, Woodard TL, Webster J, Lovley DR. 2006. Microarray and genetic analysis of electron transfer to electrodes in Geobacter sulfurreducens. Environ. Microbiol. 8:1805-1815. http://dx.doi.org/10.1111/j.1462-2920.2006.01065.x.
20. Aklujkar M, Coppi MV, Leang C, Kim BC, Chavan MA, Perpetua LA, Giloteaux L, Liu A, Holmes DE. 2013. Proteins involved in electron transfer to Fe(III) and Mn(IV) oxides by Geobacter sulfurreducens and Geobacter uraniireducens. Microbiology 159:515-535. http://dx.doi.org/10.1099/mic.0.064089-0.
21. Rollefson JB, Levar CE, Bond DR. 2009. Identification of genes involved in biofilm formation and respiration via mini-Himar transposon mutagenesis of Geobacter sulfurreducens. J. Bacteriol. 191:4207-4217. http://dx.doi.org/10.1128/JB.00057-09.
22. Mahadevan R, Palsson BØ, Lovley DR. 2011. In situ to in silico and back: elucidating the physiology and ecology of Geobacter spp. using genomescale modelling. Nat. Rev. Microbiol. 9:39-50. http://dx.doi.org/10.1038/nrmicro2456.
23. Lovley DR. 2006. Bug juice: harvesting electricity with microorganisms. Nat. Rev. Microbiol. 4:497-508. http://dx.doi.org/10.1038/nrmicro1442.
24. 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. 65:12-20. http://dx.doi.org/10.1111/j.1365-2958.2007.05783.x.
25. Liu Y, Wang Z, Liu J, Levar CE, Edwards MJ, Babauta JT, Kennedy DW, Shi Z, Beyenal H, Bond DR, Clarke TA, Butt JN, Richardson DJ, Rosso KM, Zachara JM, Fredrickson JK, Shi L. 2014. A trans-outer membrane porin-cytochrome protein complex for extracellular electron transfer by Geobacter sulfurreducens PCA. Environ. Microbiol. Rep., in press. http://dx.doi.org/10.1111/1758-2229.12204.
26. Yoho RA, Popat SC, Torres CI. 2014. Dynamic potential-dependent electron transport pathway shifts in anode biofilms of Geobacter sulfurreducens. ChemSusChem, in press. http://dx.doi.org/10.1002/cssc.201402589.
27. Cornell RM, Schwertmann U. 2003. The iron oxides: structure, properties, reactions, occurrences and uses, 2nd ed. Wiley-VCH VerlagGmbH& Co. KGaA, Weinheim, Germany.
28. Majzlan J. 2012. Minerals and aqueous species of iron and manganese as reactants and products of microbial metal respiration, p 112-28. In Gescher J, Kappler A (ed), Microbial metal respiration; from geochemistry to potential applications, 1st ed. Springer Verlag, New York, NY.
29. Thamdrup B. 2000. Bacterial manganese and iron reduction in aquatic sediments, p 4112-84. In Schink B (ed), Advances in Microbial Ecology, 16th ed. Springer Verlag, New York, NY.
30. Simon J, Gross R, Einsle O, Kroneck PM, Kröger A, Klimmek O. 2000. A NapC/NirT-type cytochrome c (NrfH) is the mediator between the quinone pool and the cytochrome c nitrite reductase of Wolinella succinogenes. Mol. Microbiol. 35:686-696. http://dx.doi.org/10.1046/j.1365-2958.2000.01742.x.
31. Yu NY, Wagner JR, Laird MR, Melli G, Rey S, Lo R, Dao P, Sahinalp SC, Ester M, Foster LJ, Brinkman FSL. 2010. PSORTb 3.0: improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes. Bioinformatics 26:1608-1615. http://dx.doi.org/10.1093/bioinformatics/btq249.
32. Boland DD, Collins RN, Glover CJ, Waite TD. 2013. An in situ quick-EXAFS and redox potential study of the Fe(II)-catalysed transformation of ferrihydrite. Colloids Surf. Physicochem. Eng. Aspects 435:2-8. http://dx.doi.org/10.1016/j.colsurfa.2013.02.009.
33. Richter H, Nevin KP, Jia H, Lowy DA, Lovley DR, Tender LM. 2009. 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. 2:506-516. http://dx.doi.org/10.1039/b816647a.
34. Marsili E, Rollefson JB, Baron DB, Hozalski RM, Bond DR. 2008. Microbial biofilm voltammetry: direct electrochemical characterization of catalytic electrode-attached biofilms. Appl. Environ. Microbiol. 74: 7329-7337. http://dx.doi.org/10.1128/AEM.00177-08.
35. Speers AM, Reguera G. 2012. Electron donors supporting growth and electroactivity of Geobacter sulfurreducens anode biofilms. Appl. Environ. Microbiol. 78:437-444. http://dx.doi.org/10.1128/AEM.06782-11.
36. Marsili E, Sun J, Bond DR. 2010. Voltammetry and growth physiology of Geobacter sulfurreducens biofilms as a function of growth stage and imposed electrode potential. Electroanalysis 22:865-874. http://dx.doi.org/10.1002/elan.200800007.
37. Rollefson JB, Stephen CS, Tien M, Bond DR. 2011. Identification of an extracellular polysaccharide network essential for cytochrome anchoring and biofilm formation in Geobacter sulfurreducens. J. Bacteriol. 193: 1023-1033. http://dx.doi.org/10.1128/JB.01092-10.
38. Coates JD, Ellis DJ, Gaw CV, Lovley DR. 1999. Geothrix fermentans gen. Nov., Sp. nov. A novel Fe(III)-reducing bacterium from a hydrocarboncontaminated aquifer. Int. J. Syst. Bacteriol. 49:1615-1622. http://dx.doi.org/10.1099/00207713-49-4-1615.
39. Podosokorskaya OA, Kadnikov VV, Gavrilov SN, Mardanov AV, Merkel AY, Karnachuk OV, Ravin NV, Bonch-Osmolovskaya EA, Kublanov IV. 2013. Characterization of Melioribacter roseus gen. nov., sp. nov., a novel facultatively anaerobic thermophilic cellulolytic bacterium from the class Ignavibacteria, and a proposal of a novel bacterial phylum Ignavibacteriae. Environ. Microbiol. 15:1759-1771. http://dx.doi.org/10.1111/1462-2920.12067.
40. Renslow R, Babauta J, Dohnalkova A, Boyanov M, Kemner K, Majors P, Fredrickson J, Beyenal H. 2013. Metabolic spatial variability in electrode-respiring Geobacter sulfurreducens biofilms. Energy Environ. Sci. 6:1827-1836. http://dx.doi.org/10.1039/c3ee40203g.
41. Bond DR, Strycharz-Glaven SM, Tender LM, Torres CI. 2012. On electron transport through Geobacter biofilms. ChemSusChem 5:1099-1105. http://dx.doi.org/10.1002/cssc.201100748.
42. 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. U. S. A. 109:15467-15472. http://dx.doi.org/10.1073/pnas.1209829109.
43. Orsetti S, Laskov C, Haderlein SB. 2013. Electron transfer between iron minerals and quinones: estimating the reduction potential of the Fe(II)-goethite surface from AQDS speciation. Environ. Sci. Technol. 47: 14161-14168. http://dx.doi.org/10.1021/es403658g.
44. Schwertmann U, Rochelle CM. 2000. Iron oxides in the laboratory: preparation and characterization. Wiley-VCH Verlag, New York, NY.
45. Mehta T, Coppi MV, Childers SE, Lovley DR. 2005. Outer membrane c-type cytochromes required for Fe(III) and Mn(IV) oxide reduction in Geobacter sulfurreducens. Appl. Environ. Microbiol. 71:8634-8641. http://dx.doi.org/10.1128/AEM.71.12.8634-8641.2005.
46. Leang C, Coppi MV, Lovley DR. 2003. OmcB, a c-type polyheme cytochrome, involved in Fe(III) reduction in Geobacter sulfurreducens. J. Bacteriol. 185:2096-2103. http://dx.doi.org/10.1128/JB.185.7.2096-2103.2003.
47. Green J, Paget MS. 2004. Bacterial redox sensors. Nat. Rev. Microbiol. 2:954-966. http://dx.doi.org/10.1038/nrmicro1022.
48. Simon J, van Spanning RJM, Richardson DJ. 2008. The organisation of proton motive and non-proton motive redox loops in prokaryotic respiratory systems. Biochim. Biophys. Acta 1777:1480-1490. http://dx.doi.org/10.1016/j.bbabio.2008.09.008.
49. Thauer RK, Kaster AK, Seedorf H, Buckel W, Hedderich R. 2008. Methanogenic archaea: ecologically relevant differences in energy conservation. Nat. Rev. Microbiol. 6:579-591. http://dx.doi.org/10.1038/nrmicro1931.
50. Kovach ME, Elzer PH, Hill DS, Robertson GT, Farris MA, Roop RM, Peterson KM. 1995. Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166:175-176. http://dx.doi.org/10.1016/0378-1119(95)00584-1.
51. Lloyd JR, Leang C, Hodges Myerson AL, Coppi MV, Cuifo S, Methe B, Sandler SJ, Lovley DR. 2003. Biochemical and genetic characterization of PpcA, a periplasmic c-type cytochrome in Geobacter sulfurreducens. Biochem. J. 369:153-161. http://dx.doi.org/10.1042/BJ20020597.
52. Khan SR, Gaines J, Roop RM, Farrand SK. 2008. Broad-host-range expression vectors with tightly regulated promoters and their use to examine the influence of TraR and TraM expression on Ti plasmid quorum sensing. Appl. Environ. Microbiol. 74:5053-5062. http://dx.doi.org/10.1128/AEM.01098-08.
53. Saltikov CW, Newman DK. 2003. Genetic identification of a respiratory arsenate reductase. Proc. Natl. Acad. Sci. U. S. A. 100:10983-10988. http://dx.doi.org/10.1073/pnas.1834303100.
54. Lovley DR, Phillips EJ. 1987. Rapid assay for microbially reducible ferric iron in aquatic sediments. Appl. Environ. Microbiol. 53:1536-1540.
55. Lovley DR, Phillips EJ. 1986. Organic matter mineralization with reduction of ferric iron in anaerobic sediments. Appl. Environ. Microbiol. 51: 683-689.