Anaerobic benzene oxidation by Geobacter species

Applied and Environmental Microbiology

Volumn 78, Issue 23, 2012, Pages 8304-8310

  Zhang, Tian ^a   Bain, Timothy S ^a   Nevin, Kelly P ^a   Barlett, Melissa A ^a   Lovley, Derek R ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHRAQUINONE-2 ,6-DISULFONATE; BENZENE DEGRADATION; BENZENE OXIDATION; CELL YIELDS; CONTAMINATED AQUIFER; ELECTRON ACCEPTOR; ELECTRON DONORS; FE REDUCTIONS; GEOBACTER; MODEL ORGANISMS; SOLE ELECTRON ACCEPTORS;

AQUIFERS; BIODEGRADATION; CARBON DIOXIDE; ELECTRONS; GROUNDWATER POLLUTION; HYDROGEOLOGY; IRON COMPOUNDS; KETONES; METABOLISM; OXIDATION; PHYSIOLOGY; STOICHIOMETRY;

BENZENE;

BACTERIAL DNA; BENZENE; CARBON DIOXIDE; FERRIC ION; GROUND WATER; RIBOSOME DNA; RNA 16S;

ABUNDANCE; ANOXIC CONDITIONS; AQUIFER POLLUTION; BACTERIUM; BENZENE; ELECTRON; GROWTH RATE; OXIDATION; STOICHIOMETRY;

ANAEROBIC GROWTH; ARTICLE; CHEMISTRY; CLASSIFICATION; CLUSTER ANALYSIS; CULTURE MEDIUM; DNA SEQUENCE; GENETICS; GEOBACTER; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; OXIDATION REDUCTION REACTION; PHYLOGENY;

ANAEROBIOSIS; BENZENE; CARBON DIOXIDE; CLUSTER ANALYSIS; CULTURE MEDIA; DNA, BACTERIAL; DNA, RIBOSOMAL; FERRIC COMPOUNDS; GEOBACTER; GROUNDWATER; MOLECULAR SEQUENCE DATA; OXIDATION-REDUCTION; PHYLOGENY; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA;

GEOBACTER; GEOBACTER METALLIREDUCENS; GEOBACTER SP.;

EID: 84870839463     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02469-12     Document Type: Article

References (68)

1. Abu Laban N, Selesi D, Jobelius C, Meckenstock RU. 2009. Anaerobic benzene degradation by Gram-positive sulfate-reducing bacteria. FEMS Microbiol. Ecol. 68:300 -311.
2. Abu Laban N, Selesi D, Rattei T, Tischler P, Meckenstock R. 2010. Identification of enzymes involved in anaerobic benzene degradation by a strictly anaerobic iron-reducing enrichment culture. Environ. Microbiol. 12:2783-2796.
3. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403- 410.
4. Amann RI, et al. 1990. Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl. Environ. Microbiol. 56:1919 -1925.
5. Anderson RT, Rooney-Varga JN, Gaw CV, Lovley DR. 1998. Anaerobic benzene oxidation in the Fe(III) reduction zone of petroleum contaminated aquifers. Environ. Sci. Technol. 32:1222-1229.
6. Botton S, Van Harmelen M, Braster M, Parsons JR, Roling WF. 2007. Dominance of Geobacteraceae in BTX-degrading enrichments from an iron-reducing aquifer. FEMS Microbiol. Ecol. 62:118 -130.
7. Butler JE, et al. 2007. Genomic and microarray analysis of aromatics degradation in Geobacter metallireducens and comparison to a Geobacter isolate from a contaminated field site.BMCGenomics 8:180. doi:10.1186/ 1471-2164-8-180.
8. Caldwell ME, Suflita JM. 2000. Detection of phenol and benzoate as intermediates of anaerobic benzene biodegradation under different terminal electron-accepting conditions. Environ. Sci. Technol. 34:1216- 1220.
9. Chakraborty R, Coates JD. 2004. Anaerobic degradation of monoaromatic hydrocarbons. Appl. Microbiol. Biotechnol. 64:437- 446.
10. Chakraborty R, Coates JD. 2005. Hydroxylation and carboxylation-two crucial steps of anaerobic benzene degradation by Dechloromonas strain RCB. Appl. Environ. Microbiol. 71:5427-5432.
11. Coates JD, et al. 2001. Anaerobic benzene oxidation coupled to nitrate reduction in pure culture by two strains of Dechloromonas. Nature 411: 1039-1043.
12. Coates JD, Chakraborty R, McInerney MJ. 2002. Anaerobic benzene biodegradation-a new era. Res. Microbiol. 153:621- 628.
13. Coates JD, Phillips EJ, Lonergan DJ, Jenter H, Lovley DR. 1996. Isolation of Geobacter species from diverse sedimentary environments. Appl. Environ. Microbiol. 62:1531-1536.
14. Coates JD, Woodward J, Allen J, Philp P, Lovley DR. 1997. Anaerobic degradation of polycyclic aromatic hydrocarbons and alkanes in petroleum-contaminated marine harbor sediments. Appl. Environ. Microbiol. 63:3589 -3593.
15. Coppi MV, Leang C, Sandler SJ, Lovley DR. 2001. Development of a genetic system for Geobacter sulfurreducens. Appl. Environ. Microbiol. 67:3180 -3187.
16. Da Silva ML, Ruiz-Aguilar GM, Alvarez PJ. 2005. Enhanced anaerobic biodegradation of BTEX-ethanol mixtures in aquifer columns amended with sulfate, chelated ferric iron or nitrate. Biodegradation 16:105-114.
17. Dou J, Liu X, Hu Z, Deng D. 2008. Anaerobic BTEX biodegradation linked to nitrate and sulfate reduction. J. Hazard. Mater. 151:720 -729.
18. Eden PA, Schmidt TM, Blakemore RP, Pace NR. 1991. Phylogenetic analysis of Aquaspirillum magnetotacticum using polymerase chain reaction-amplified 16S rRNA-specific DNA. Int. J. Syst. Bacteriol. 41:324- 325.
19. Ettwig KF, et al. 2010. Nitrite-driven anaerobic methane oxidation by oxygenic bacteria. Nature 464:543-548.
20. Farhadian M, Vachelard C, Duchez D, Larroche C. 2008. In situ bioremediation of monoaromatic pollutants in groundwater: a review. Bioresour. Technol. 99:5296 -5308.
21. Fischer A, et al. 2008. Combined carbon and hydrogen isotope fractionation investigations for elucidating benzene biodegradation pathways. Environ. Sci. Technol. 42:4356-4363.
22. Gouy M, Guindon S, Gascuel O. 2010. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol. Biol. Evol. 27:221-224.
23. Grbic-Galic D, Vogel TM. 1987. Transformation of toluene and benzene by mixed methanogenic cultures. Appl. Environ. Microbiol. 53:254 -260.
24. Hayes LA, Nevin KP, Lovley DR. 1999. Role of prior exposure on anaerobic degradation of naphthalene and phenanthrene in marine harbor sediments. Org. Geochem. 30:937-945.
25. Holmes DE, Nevin KP, Lovley DR. 2004. Comparison of 16S rRNA, nifD, recA, gyrB, rpoB, and fusA genes within the family Geobacteraceae fam. nov. Int. J. Syst. Evol. Microbiol. 54:1591-1599.
26. Holmes DE, et al. 2007. Subsurface clade of Geobacteraceae that predominates in a diversity of Fe(III)-reducing subsurface environments. ISME J. 1:663- 677.
27. Holmes DE, Risso C, Smith JA, Lovley DR. 2011. Anaerobic oxidation of benzene by the hyperthermophilic archaeon Ferroglobus placidus. Appl. Environ. Microbiol. 77:5926 -5933.
28. Holmes DE, Risso C, Smith JA, Lovley DR. 2012. Genome-scale analysis of anaerobic benzoate and phenol metabolism in the hyperthermophilic archaeon Ferroglobus placidus. ISME J. 6:146 -157.
29. Jin S, Fallgren PH, Bilgin AA, Morris JM, Barnes PW. 2007. Bioremediation of benzene, ethylbenzene, and xylenes in groundwater under ironamended, sulfate-reducing conditions. Environ. Toxicol. Chem. 26:249- 253.
30. Jindrova E, Chocova M, Demnerova K, Brenner V. 2002. Bacterial aerobic degradation of benzene, toluene, ethylbenzene and xylene. Folia Microbiol. (Praha) 47:83-93.
31. Kasai Y, Kodama Y, Takahata Y, Hoaki T, Watanabe K. 2007. Degradative capacities and bioaugmentation potential of an anaerobic benzenedegrading bacterium strain DN11. Environ. Sci. Technol. 41:6222- 6227.
32. Kasai Y, Takahata Y, Manefield M, Watanabe K. 2006. RNA-based stable isotope probing and isolation of anaerobic benzene-degrading bacteria from gasoline-contaminated groundwater. Appl. Environ. Microbiol. 72:3586 -3592.
33. Kashefi K, Holmes DE, Baross JA, Lovley DR. 2003. Thermophily in the Geobacteraceae: Geothermobacter ehrlichii gen. nov., sp. nov., a novel thermophilic member of the Geobacteraceae from the "Bag City" hydrothermal vent. Appl. Environ. Microbiol. 69:2985-2993.
34. Kunapuli U, Griebler C, Beller HR, Meckenstock RU. 2008. Identification of intermediates formed during anaerobic benzene degradation by an iron-reducing enrichment culture. Environ. Microbiol. 10:1703-1712.
35. Lane DJ, et al. 1985. Rapid determination of 16S rRNA sequences for phylogenetic analyses. Proc. Natl. Acad. Sci. U. S. A. 82:6955- 6959.
36. Lin B, Van Verseveld HW, Roling WF. 2002. Microbial aspects of anaerobic BTEX degradation. Biomed. Environ. Sci. 15:130 -144.
37. Lovley DR. 2000. Anaerobic benzene degradation. Biodegradation 11: 107-116.
38. Lovley DR. 1997. Potential for anaerobic bioremediation of BTEX in petroleum-contaminated aquifers. J. Ind. Microbiol. Biotechnol. 18: 75- 81.
39. Lovley DR, et al. 1989. Oxidation of aromatic contaminants coupled to microbial iron reduction. Nature 339:297-300.
40. Lovley DR, Coates JD, BluntHarris EL, Phillips EJP, Woodward JC. 1996. Humic substances as electron acceptors for microbial respiration. Nature 382:445- 448.
41. Lovley DR, et al. 1993. Geobacter metallireducens gen. nov. sp. nov., a microorganism capable of coupling the complete oxidation of organic compounds to the reduction of iron and other metals. Arch. Microbiol. 159:336 -344.
42. Lovley DR, Lonergan DJ. 1990. Anaerobic oxidation of toluene, phenol, and p-cresol by the dissimilatory iron-reducing organism, GS-15. Appl. Environ. Microbiol. 56:1858 -1864.
43. Lovley DR, Phillips EJ. 1988. Novel mode of microbial energy metabolism: organic carbon oxidation coupled to dissimilatory reduction of iron or manganese. Appl. Environ. Microbiol. 54:1472-1480.
44. Lovley DR, et al. 2011. Geobacter: the microbe electric's physiology, ecology, and practical applications Adv. Microb. Physiol. 59:1-100.
45. Lovley DR, Woodward JC, Chapelle FH. 1996. Rapid anaerobic benzene oxidation with a variety of chelated Fe(III) forms. Appl. Environ. Microbiol. 62:288 -291.
46. Lovley DR, Woodward JC, Chapelle FH. 1994. Stimulated anoxic biodegradation of aromatic hydrocarbons using Fe(III) ligands. Nature 370: 128-131.
47. Meckenstock RU, Mouttaki H. 2011. Anaerobic degradation of nonsubstituted aromatic hydrocarbons. Curr. Opin. Biotechnol. 22:406-414.
48. Nevin KP, et al. 2005. Geobacter bemidjiensis sp. nov. and Geobacter psychrophilus sp. nov., two novel Fe(III)-reducing subsurface isolates. Int. J. Syst. Evol. Microbiol. 55:1667-1674.
49. Oberender J, Kung J, Seifert J, Von Bergen M, Boll M. 2012. Identification and characterization of a succinyl-CoA: benzoate CoA transferase in Geobacter metallireducens. J. Bacteriol. 194:2501-2508.
50. Phelps CD, Young LY. 1999. Anaerobic biodegradation of BTEX and gasoline in various aquatic sediments. Biodegradation. 10:15-25.
51. Phelps CD, Zhang X, Young LY. 2001. Use of stable isotopes to identify benzoate as a metabolite of benzene degradation in a sulphidogenic consortium. Environ. Microbiol. 3:600-603.
52. Prakash O, et al. 2010. Geobacter daltonii sp. nov., an Fe(III)- and uranium( VI)-reducing bacterium isolated from a shallow subsurface exposed to mixed heavy metal and hydrocarbon contamination. Int. J. Syst. Evol. Microbiol. 60:546 -553.
53. Röling WF, Van Breukelen BM, Braster M, Lin B, Van Verseveld HW. 2001. Relationships between microbial community structure and hydrochemistry in a landfill leachate-polluted aquifer. Appl. Environ. Microbiol. 67:4619-4629.
54. Rooney-Varga JN, Anderson RT, Fraga JL, Ringelberg D, Lovley DR. 1999. Microbial communities associated with anaerobic benzene degradation in a petroleum-contaminated aquifer. Appl. Environ. Microbiol. 65:3056 -3063.
55. Salinero KK, et al. 2009. Metabolic analysis of the soil microbe Dechloromonas aromatica str. RCB: indications of a surprisingly complex lifestyle and cryptic anaerobic pathways for aromatic degradation. BMC Genomics 10:351. doi:10.1186/1471-2164-10-351.
56. Staats M, Braster M, Rölling WF. 2011. Molecular diversity and distribution of aromatic hydrocarbon-degrading anaerobes across a landfill leachate plume. Environ. Microbiol. 13:1216 -1227.
57. Staudinger J, Roberts PV. 1996. A critical review of Henry's law constants for environmental applications. Crit. Rev. Environ. Sci. Technol. 26:205-297.
58. Tobler NB, Hofstetter TB, Straub KL, Fontana D, Schwarzenbach RP. 2007. Iron-mediated microbial oxidation and abiotic reduction of organic contaminants under anoxic conditions. Environ. Sci. Technol. 41:7765-7772.
59. Tremblay PL, Aklujkar M, Leang C, Nevin KP, Lovley DR. 2011. A genetic system for Geobacter metallireducens: role of the flagellin and pilin in the reduction of Fe(III) oxide. Environ. Microbiol. Rep. 4:82- 88.
60. 6-benzene in nitrate-reducing and methanogenic enrichment cultures. Environ. Sci. Technol. 39:6681- 6691.
61. Vogel TM, Grbic-Galic D. 1986. Incorporation of oxygen from water into toluene and benzene during anaerobic fermentative transformation. Appl. Environ. Microbiol. 52:200 -202.
62. Vogt C, Kleinsteuber S, Richnow HH. 2011. Anaerobic benzene degradation by bacteria. Microb. Biotechnol. 4:710 -724.
63. Weelink SA, et al. 2008. Isolation and characterization of Alicycliphilus denitrificans strain BC, which grows on benzene with chlorate as the electron acceptor. Appl. Environ. Microbiol. 74:6672- 6681.
64. Weelink SAB, Van Eekert MHA, Stams AJM. 2010. Degradation of BTEX by anaerobic bacteria: physiology and application. Rev. Environ. Sci. Biotechnol. 9:359 -385.
65. Weiner JM, Lovley DR. 1998. Anaerobic benzene degradation in petroleum-contaminated aquifer sediments after inoculation with a benzeneoxidizing enrichment. Appl. Environ. Microbiol. 64:775-778.
66. Wilson LP, Bouwer EJ. 1997. Biodegradation of aromatic compounds under mixed oxygen/denitrifying conditions: a review. J. Ind. Microbiol. Biotechnol. 18:116 -130.
67. Yun J, Ueki T, Miletto M, Lovley DR. 2011. Monitoring the metabolic status of Geobacter species in contaminated groundwater by quantifying key metabolic proteins with Geobacter-specific antibodies. Appl. Environ. Microbiol. 77:4597- 4602.
68. Zedelius J, et al. 2011. Alkane degradation under anoxic conditions by a nitrate-reducing bacterium with possible involvement of the electron acceptor in substrate activation. Environ. Microbiol. Rep. 3:125-135.