Bacterial community structure, compartmentalization and activity in a microbial fuel cell

Journal of Applied Microbiology

Volumn 101, Issue 3, 2006, Pages 698-710

  Kim, G T ^a   Webster, G ^a,d   Wimpenny, J W T ^a   Kim, B H ^b   Kim, H J ^c   Weightman, A J ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b Korea Institute of Science and Technology   (South Korea)

^c Konkuk University   (South Korea)

^d CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

16S rRNA; Anaerobic respiration; Biofilm; Denaturing gradient gel electrophoresis; Electrochemical activity; Fe(III) reducing bacteria; Klebsiella oxytoca; Microbial fuel cell

Indexed keywords

BIOFILMS; ELECTRODES; ELECTROPHORESIS; GENES; IRON COMPOUNDS; LIBRARIES; MICROBIAL FUEL CELLS; RNA;

16S RRNA; 16S RRNA GENE; ANAEROBIC RESPIRATION; BACTERIAL COMMUNITY STRUCTURE; DENATURING GRADIENT GEL ELECTROPHORESIS; ELECTROCHEMICAL ACTIVITIES; FE(III)-REDUCING BACTERIA; GAMMAPROTEOBACTERIA; KLEBSIELLA OXYTOCA; RRNA GENE LIBRARY;

BACTERIA;

DNA; IRON; NUCLEOTIDE; RIBOSOME RNA;

BACTERIUM; BIOFILM; COMMUNITY STRUCTURE; COMPARTMENTALIZATION; ELECTRODE; ELECTRON MICROSCOPY; GENE; MICROBIAL COMMUNITY; RNA;

AGAR GEL ELECTROPHORESIS; ARTICLE; BACTERIAL FLORA; BIOFILM; CELL COMPARTMENTALIZATION; CYCLIC POTENTIOMETRY; DENATURING GRADIENT GEL ELECTROPHORESIS; ELECTROCHEMISTRY; ELECTRON MICROSCOPY; ENTEROBACTER; ENTEROBACTERIACEAE; GAMMAPROTEOBACTERIA; GENE LIBRARY; GENE SEQUENCE; KLEBSIELLA; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PLANKTON; POLYMERASE CHAIN REACTION; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; UNINDEXED SEQUENCE;

BACTERIA (MICROORGANISMS); ENTEROBACTER SP.; ENTEROBACTERIACEAE; GAMMAPROTEOBACTERIA; KLEBSIELLA SP.;

EID: 33747099503     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/j.1365-2672.2006.02923.x     Document Type: Article

References (55)

1. Allen, R.M. and Bennetto, H.P. (1993) Microbial fuel cells: electricity production from carbohydrates. Appl Biochem Biotechnol 39, 27-40.
2. Baldi, F., Minacci, A., Pepi, M. and Scozzafava, A. (2001) Gel sequestration of heavy metals by Klebsiella oxytoca isolated from iron mat. FEMS Microbiol Ecol 36, 169-174.
3. Blackall, L.L., Burrell, P.C., Gwilliam, H., Bradford, D., Bond, P.L. and Hugenholtz, P. (1998) The use of 16S rDNA clone libraries to describe the microbial diversity of activated sludge communities. Water Sci Technol 37, 451-454.
4. Bond, D.R. and Lovley, D.R. (2003) Electricity production by Geobacter sulfurreducens attached to electrodes. Appl Environ Microbiol 69, 1548-1555.
5. Bond, D.R., Holmes, D.E., Tender, L.M. and Lovley, D.R. (2002) Electrode-reducing microorganisms that harvest energy from marine sediments. Science 295, 483-485.
6. Caccavo, F., Coates, J.D., Rossello-Mora, R.A., Ludwig, W., Schleifer, K.-H., Lovley, D.R. and McInerney, M.J. (1996) Geovibrio ferrireducens, a phylogenetically distinct dissimilatory Fe(III)-reducing bacterium. Arch Microbiol 165, 370-376.
7. Caldwell, D.E., Korber, D.R. and Lawrence, J.R. (1992) Imaging of bacterial cells by fluorescence exclusion using scanning confocal laser microscopy. J Microbiol Methods 15, 249-261.
8. Chaudhuri, S.K. and Lovley, D.R. (2003) Electricity generation by direct oxidation of glucose in mediatorless microbial fuel cells. Nat Biotechnol 21, 1229-1232.
9. Coates, J.D., Phillips, E.J.P., Lonergan, D.J., Jenter, H. and Lovley, D.R. (1996) Isolation of Geobacter species from diverse sedimentary environments. Appl Environ Microbiol 62, 1531-1536.
10. Delaney, G.M., Bennetto, H.P., Mason, J.R., Roller, S.D., Stirling, J.L. and Thurston, C.F. (1984) Electron-transfer coupling in microbial fuel cells: 2. Performance of fuel cells containing selected microorganism-mediator substrate combinations. J Chem Technol Biotechnol 34B, 13-27.
11. Eschenhagen, M., Schuppler, M. and Röske, I. (2003) Molecular characterization of the microbial community structure in two activated sludge systems for the advanced treatment of domestic effluents. Water Res 37, 3224-3232.
12. Felsenstein, J. (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783-791.
13. Gregory, K.B., Bond, D.R. and Lovley, D.R. (2004) Graphite electrodes as electron donor for anaerobic respiration. Environ Microbiol 6, 596-604.
14. Holmes, D.E., Bond, D.R. and Lovley, D.R. (2004a) Electron transfer by Desulfobulbus propionicus to Fe(III) and graphite electrodes. Appl Environ Microbiol 70, 1234-1237.
15. Holmes, D.E., Bond, D.R., O'Neil, R.A., Reimers, C.E., Tender, L.R. and Lovley, D.R. (2004b) Microbial communities associated with electrodes harvesting electricity from a variety of aquatic sediments. Microb Ecol 48, 178-190.
16. Holmes, D.E., Nicoll, J.S., Bond, D.R. and Lovley, D.R. (2004c) Potential role of a novel Psychrotolerant member of the family Geobacteraceae, Geopsychrobacter electrodiphilus gen. nov., sp. nov., in electricity production by a marine sediment fuel cell. Appl Environ Microbiol 70, 6023-6030.
17. Hugenholtz, P., Tyson, G.W., Webb, R.I., Wagner, A.M. and Blackall, L.L. (2001) Investigation of candidate division TM7, a recently recognized major lineage of the domain bacteria with no known pure-culture representatives. Appl Environ Microbiol 67, 411-419.
18. Hungate, R.E. (1969) A roll tube method for cultivation of strict anaerobes. In Methods in Microbiology 3B ed. Norris, J.R. and Ribbons, E.W. pp. 117-132. New York, USA: Academic Press.
19. Hyun, M.S., Kim, B.H., Chang, I.S., Park, H.S., Kim, H.J., Kim, G.T., Kim, M. and Park, D.H. (1999) Isolation and identification of an anaerobic dissimilatory Fe(III)-reducing bacterium, Shewanella putrefaciens IR-1. J Microbiol 37, 206-212.
20. Jukes, T.H. and Cantor, C.R. (1969) Evolution of protein molecules. In Mammalian Protein Metabolism ed. Munro, H.N. pp. 21-132. New York, USA: Academic Press.
21. Kemp, P.F. and Aller, J.Y. (2004) Bacterial diversity in aquatic and other environments: what 16S rDNA libraries can tell us. FEMS Microbiol Ecol 47, 161-177.
22. Kim, T.S. and Kim, B.H. (1988) Modulation of Clostridium acetobutylicum fermentation by electrochemically supplied reducing equivalent. Biotechnol Lett 10, 123-128.
23. Kim, B.H., Kim, H.J., Hyun, M.S. and Park, D.H. (1999a) Direct electrode reaction of Fe(III)-reducing bacterium, Shewanella putrefaciens. J Microbiol Biotechnol 9, 127-131.
24. Kim, H.J., Hyun, M.S., Chang, I.S. and Kim, B.H. (1999b) A microbial fuel cell type lactate biosensor using a metal-reducing bacterium, Shewanella putrefaciens. J Microbiol Biotechnol 9, 365-367.
25. Kim, N., Choi, Y., Jung, S. and Kim, S. (2000) Effect of initial carbon sources on the performance of microbial fuel cells containing Proteous vulgaris. Biotechnol Bioeng 70, 109-114.
26. Kim, H.J., Park, H.S., Hyun, M.S., Chang, I.S., Kim, M. and Kim, B.H. (2002) A mediator-less microbial fuel cell using a metal reducing bacterium, Shewanella putrefaciens. Enzyme Microb Technol 30, 145-152.
27. Kim, B.H., Park, H.S., Kim, H.J., Kim, G.T., Chang, I.S., Lee, J. and Phung, N.T. (2004) Enrichment of microbial community generating electricity using a fuel-cell-type electrochemical cell. Appl Microbiol Biotechnol 63, 672-681.
28. Kim, G.T., Hyun, M.S., Chang, I.S., Kim, H.J., Park, H.S., Kim, B.H., Kim, S.D., Wimpenny, J.W.T. et al. (2005) Dissimilatory Fe(III) reduction by electrochemically active lactic acid bacterium phylogenetically related to Enterococcus gallinarum isolated from submerged soil. J Appl Microbiol 99, 978-987.
29. Knight, V. and Blakemore, R. (1998) Reduction of diverse electron acceptors by Aeromonas hydrophila. Arch Microbiol 169, 239-248.
30. Lane, D.J. (1991) 16S/23S rRNA sequencing. In Nucleic Acid Techniques in Bacterial Systematics ed. Stackebrandt, E. and Goodfellow, M. pp. 115-175. New York, USA: John Wiley and Sons.
31. Lee, J., Phung, N.T., Chang, I.S., Kim, B.H. and Sung, H.C. (2003) Use of acetate for enrichment of electrochemically active microorganisms and their 16S rDNA analyses. FEMS Microbiol Lett 223, 185-191.
32. Lovley, D.R., Phillips, E.J.P. and Lonergan, D.J. (1989) Hydrogen and formate oxidation coupled to dissimilatory reduction of iron or manganese by Alteromonas putrefaciens. Appl Environ Microbiol 55, 700-706.
33. Lovley, D.R., Caccavo, F. and Phillips, E.J.P. (1992) Acetate oxidation by dissimilatory Fe(III) reducers. Appl Environ Microbiol 58, 3205-3206.
34. Lovley, D.R., Giovannoni, S.J., White, D.C., Champine, J.E., Phillips, E.J.P., Gorby, Y.A. and Goodwin, S. (1993) Geobacter metallireducens gen. nov. sp. now., a microorganism capable of coupling the complete oxidation of organic compounds to the reduction of iron, and other metals. Arch Microbiol 159, 336-344.
35. Lovley, D.R., Holmes, D.E. and Nevin, K.P. (2004) Dissimilatory Fe(III) and Mn(IV) reduction. Adv Microb Physiol 49, 219-286.
36. McCaig, A.E., Embley, T.M. and Prosser, J.I. (1994) Molecular analysis of enrichment cultures of marine ammonia oxidizers. FEMS Microbiol Lett 120, 363-368.
37. McKinlay, J.B. and Zeikus, J.G. (2004) Extracellular iron reduction is mediated in part by neutral red and hydrogenase in Escherichia coli. Appl Environ Microbiol 70, 3467-3474.
38. McLaughlin, J.R., Ryden, J.C. and Syers, J.K. (1981) Sorption of inorganic phosphate by iron- and aluminum-containing components. J Soil Sci 32, 365-377.
39. Muyzer, G., de Waal, E.C. and Uitterlinden, A.G. (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for16S rRNA. Appl Environ Microbiol 59, 695-700.
40. Myers, C.R. and Myers, J.M. (1992) Localization of cytochromes to the outer membrane of anaerbically grown Shewanella putrefaciens MR-1. J Bacteriol 174, 3429-3438.
41. Nielsen, J.L., Juretschko, S., Wagner, M. and Nielsen, P.H. (2002) Abundance and phylogenetic affiliation of iron reducers in activated sludge as assessed by fluorescence in situ hybridization and microautoradiography. Appl Environ Microbiol 68, 4629-4636.
42. Park, D.H. and Zeikus, J.G. (2000) Electricity generation in microbial fuel cells using neutral red as an electronophore. Appl Environ Microbiol 66, 1292-1297.
43. Park, H.S., Kim, B.H., Kim, H.S., Kim, H.J., Kim, G.T., Kim, M., Chang, I.S., Park, Y.K. et al. (2001) A novel electrochemically active and Fe(III) reducing bacterium phylogenetically related to Clostridium butyricum isolated from a bacterial fuel cell. Anaerobe 7, 297-306.
44. van de Peer, Y. and De Wachter, R. (1994) TREECON for Windows: a software package for the construction and drawing of evolutionary trees for Microsoft Windows environment. Comput Appl Biosci 10, 569-570.
45. Pham, C.A., Jung, S.J., Phung, N.T., Lee, J., Chang, I.S., Kim, B.H., Yi, H. and Chun, J. (2003) A novel electrochemically active and Fe(III)-reducing bacterium phylogenetically related to Aeromonas hydrophila, isolated from a microbial fuel cell. FEMS Microbiol Lett 223, 129-134.
46. Phillips, E.J.P. and Lovley, D.R. (1987) Determination of Fe(III) and Fe(II) in oxalate extract of sediment. Soil Sci Soc Am J 51, 938-941.
47. Rabaey, K., Boon, N., Siciliano, S.D., Verhaege, M. and Verstraete, W. (2004) Biofuel cells select for microbial consortia that self-mediate electron transfer. Appl Environ Microbiol 70, 5373-5382.
48. Reguera, G., McCarthy, K.D., Mehta, T., Nicoll, J.S., Tuominen, M.T. and Lovley, D.R. (2005) Extracellular electron transfer via microbial nanowires. Nature 435, 1098-1101.
49. Schink, B. and Bomar, M. (1992) The genera Acetobacterium, Acetogenium, Acetoanaerobium and Acetitomaculum. In The Prokaryotes ed. Balows, A., Trueper, H.G., Dworkin, M., Harder, W. and Schleifer, K.-H. pp. 1923-1936. New York, USA: Springer.
50. Sheffield, V.C., Cox, D.R., Lerman, L.S. and Myers, R.M. (1989) Attachment of a 40-base pair G + C rich sequence (GC-clamp) to genomic DNA fragments by the polymerase chain reaction results in improved detection of single-base changes. Proc Natl Acad Sci U S A 86, 232-236.
51. Snaidr, J., Amann, R., Huber, I., Ludwig, W. and Schleifer, K.-H. (1997) Phylogenetic analysis and in situ identification of bacteria in activated sludge. Appl Environ Microbiol 63, 2884-2896.
52. Tebo, B.M. and Obraztsova, A.Y. (1998) Sulfate-reducing bacterium grows with Cr(VI), U(VI), Mn(IV), and Fe(III) as electron acceptors. FEMS Microbiol Lett 162, 193-198.
53. Tender, L.M., Reimers, C.E., Stecher, H.A. III, Holmes, D.E., Bond, D.R., Lowy, D.A., Pilobello, K., Fertig, S.J. et al. (2002) Harnessing microbially generating power on the seafloor. Nat Biotechnol 20, 821-825.
54. Webster, G., Newberry, C.J., Fry, J.C. and Weightman, A.J. (2003) Assessment of bacterial community structure in the deep sub-seafloor biosphere by 16S rDNA-based techniques: a cautionary tale. J Microbiol Methods 55, 155-164.
55. Zhou, J., Bruns, M.A. and Tiedje, J.M. (1996) DNA recovery from soils of diverse composition. Appl Environ Microbiol 62, 316-322.