Anaerobic benzene oxidation via phenol in Geobacter metallireducens

Applied and Environmental Microbiology

Volumn 79, Issue 24, 2013, Pages 7800-7806

  Zhang, Tian ^a   Tremblay, Pier Luc ^a   Chaurasia, Akhilesh Kumar ^a   Smith, Jessica A ^a   Bain, Timothy S ^a   Lovley, Derek R ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BENZENE DEGRADATION; BENZENE HYDROXYLATION; BENZENE OXIDATION; BENZENE TO PHENOL; CELL-FREE CONTROLS; ENVIRONMENTAL SIGNIFICANCE; GENE EXPRESSION PATTERNS; GEOBACTER SULFURREDUCENS;

BIODEGRADATION; CARBON DIOXIDE; CARBOXYLATION; CHEMICALS REMOVAL (WATER TREATMENT); GENE EXPRESSION; GROUNDWATER; METABOLISM; PHENOLS; PHYSIOLOGY;

BENZENE;

BENZENE; BIOCHEMISTRY; BIODEGRADATION; ENZYME ACTIVITY; GENETIC ANALYSIS; GROIN; GROUNDWATER; METABOLISM; MICROBIAL ACTIVITY; OXIDATION; TOLUENE; WATER POLLUTION;

BENZENE; CARBON DIOXIDE; IRON; PHENOL; WATER;

ANAEROBIC GROWTH; ARTICLE; GENE DELETION; GENE EXPRESSION PROFILING; GENETICS; GEOBACTER; METABOLISM; OXIDATION REDUCTION REACTION;

ANAEROBIOSIS; BENZENE; CARBON DIOXIDE; GENE DELETION; GENE EXPRESSION PROFILING; GEOBACTER; IRON; METABOLIC NETWORKS AND PATHWAYS; OXIDATION-REDUCTION; PHENOL; WATER;

EID: 84888267751     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.03134-13     Document Type: Article

References (71)

1. Vogt C, Kleinsteuber S, Richnow HH. 2011. Anaerobic benzene degradation by bacteria. Microb. Biotechnol. 4:710-724.
2. Carmona M, Zamarro MT, Blazquez B, Durante-Rodriguez G, Juarez JF, Valderrama JA, Barragan MJ, Garcia JL, Diaz E. 2009. Anaerobic catabolism of aromatic compounds: a genetic and genomic view. Microbiol. Mol. Biol. Rev. 73:71-133.
3. Foght J. 2008. Anaerobic biodegradation of aromatic hydrocarbons: pathways and prospects. J. Mol. Microbiol. Biotechnol. 15:93-120.
4. Fuchs G. 2008. Anaerobic metabolism of aromatic compounds. Ann. N. Y. Acad. Sci. 1125:82-99.
5. Anderson RT, Lovley DR. 2000. Anaerobic bioremediation of benzene under sulfate-reducing conditions in a petroleum-contaminated aquifer. Environ. Sci. Technol. 34:2261-2266.
6. 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.
7. Coates JD, Chakraborty R, McInerney MJ. 2002. Anaerobic benzene biodegradation-a new era. Res. Microbiol. 153:621-628.
8. Lovley DR, Coates JD, Woodward JC, Phillips E. 1995. Benzene oxidation coupled to sulfate reduction. Appl. Environ. Microbiol. 61:953-958.
9. Meckenstock RU, Mouttaki H. 2011. Anaerobic degradation of nonsubstituted aromatic hydrocarbons. Curr. Opin. Biotechnol. 22:406-414.
10. 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.
11. 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.
12. Weiner JM, Lovley DR. 1998. Rapid benzene degradation in methanogenic sediments from a petroleum-contaminated aquifer. Appl. Environ. Microbiol. 64:1937-1939.
13. 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.
14. Lovley DR, Woodward JC, Chapelle FH. 1994. Stimulated anoxic biodegradation of aromatic hydrocarbons using Fe(III) ligands. Nature 370: 128-131.
15. Lovley DR, Coates JD, Blunt-Harris EL, Phillips EJP, Woodward JC. 1996. Humic substances as electron acceptors for microbial respiration. Nature 382:445-448.
16. Zhang T, Gannon SM, Nevin KP, Franks AE, Lovley DR. 2010. Stimulating the anaerobic degradation of aromatic hydrocarbons in contaminated sediments by providing an electrode as the electron acceptor. Environ. Microbiol. 12:1011-1020.
17. 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.
18. 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.
19. 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.
20. 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.
21. 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.
22. Musat F, Widdel F. 2008. Anaerobic degradation of benzene by a marine sulfate-reducing enrichment culture, and cell hybridization of the dominant phylotype. Environ. Microbiol. 10:10-19.
23. 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.
24. 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.
25. Coates JD, Chakraborty R, Lack JG, O'Connor SM, Cole KA, Bender KS, Achenbach LA. 2001. Anaerobic benzene oxidation coupled to nitrate reduction in pure culture by two strains of Dechloromonas. Nature 411: 1039-1043.
26. Salinero KK, Keller K, Feil WS, Feil H, Trong S, Di Bartolo G, Lapidus A. 2009. Metabolic analysis of the soil microbe Dechloromonas aromatica str. RCB: indications of a surprisingly complex life-style and cryptic anaerobic pathways for aromatic degradation. BMC Genomics 10:351. doi: 101186./1471-2164-10-351.
27. Weelink SAB, van Eekert MHA, Stams AJM. 2010. Degradation of BTEX by anaerobic bacteria: physiology and application. Rev. Environ. Sci. Biotechnol. 9:359-385.
28. Ulrich AC, Beller HR, Edwards EA. 2005. Metabolites detected during biodegradation of 13C6-benzene in nitrate-reducing and methanogenic enrichment cultures. Environ. Sci. Technol. 39:6681-6691.
29. 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.
30. 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.
31. 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.
32. Holmes DE, O'Neil RA, Vrionis HA, N'Guessan AL, Ortiz-Bernad I, Larrahondo MJ, Adams LA, Ward JA, Nicoll JS, Nevin KP, Chavan MA, Johnson JP, Long PE, Lovley DR. 2007. Subsurface clade of Geobacteraceae that predominates in a diversity of Fe(III)-reducing subsurface environments. ISME J. 1:663-677.
33. Hosoda A, Kasai Y, Hamamura N, Takahata Y, Watanabe K. 2005. Development of a PCR method for the detection and quantification of benzoyl-CoA reductase genes and its application to monitored natural attenuation. Biodegradation 16:591-601.
34. Kane SR, Beller HR, Legler TC, Anderson RT. 2002. Biochemical and genetic evidence of benzylsuccinate synthase in toluene-degrading, ferric iron-reducing Geobacter metallireducens. Biodegradation 13:149-154.
35. Kuntze K, Vogt C, Richnow HH, Boll M. 2011. Combined application of PCR-based functional assays for the detection of aromatic-compounddegrading anaerobes. Appl. Environ. Microbiol. 77:5056-5061.
36. Lovley DR, Baedecker MJ, Lonergan DJ, Cozzarelli IM, Phillips EJP, Siegel DI. 1989. Oxidation of aromatic contaminants coupled to microbial iron reduction. Nature 339:297-300.
37. Lovley DR, Ueki T, Zhang T, Malvankar NS, Shrestha PM, Flanagan K, Aklujkar M, Butler JE, Giloteaux L, Rotaru AE, Holmes DE, Franks AE, Orellana R, Risso C, Nevin KP. 2011. Geobacter: the microbe electric's physiology, ecology, and practical applications. Adv. Microb. Physiol. 59: 1-100.
38. 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.
39. 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.
40. 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.
41. 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.
42. Winderl C, Anneser B, Griebler C, Meckenstock RU, Lueders T. 2008. Depth-resolved quantification of anaerobic toluene degraders and aquifer microbial community patterns in distinct redox zones of a tar oil contaminant plume. Appl. Environ. Microbiol. 74:792-801.
43. 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.
44. Zhang T, Bain TS, Nevin KP, Barlett MA, Lovley DR. 2012. Anaerobic benzene oxidation by Geobacter species. Appl. Environ. Microbiol. 78: 8304-8310.
45. Tremblay PL, Aklujkar M, Leang C, Nevin KP, Lovley DR. 2012. 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.
46. Lovley DR, Giovannoni SJ, White DC, Champine JE, Phillips EJP, Gorby YA, Goodwin S. 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.
47. 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.
48. Holmes DE, Nevin KP, O'Neil RA, Ward JE, Adams LA, Woodard TL, Vrionis HA, Lovley DR. 2005. Potential for quantifying expression of the Geobacteraceae citrate synthase gene to assess the activity of Geobacteraceae in the subsurface and on current-harvesting electrodes. Appl. Environ. Microbiol. 71:6870-6877.
49. -ΔΔCT method. Methods 25: 402-408.
50. Kim BC, Leang C, Ding YH, Glaven RH, Coppi MV, Lovley DR. 2005. OmcF, a putative c-type monoheme outer membrane cytochrome required for the expression of other outer membrane cytochromes in Geobacter sulfurreducens. J. Bacteriol. 187:4505-4513.
51. Marx CJ, Lidstrom ME. 2001. Development of improved versatile broadhost-range vectors for use in methylotrophs and other Gram-negative bacteria. Microbiology 147:2065-2075.
52. Lovley DR, Phillips EJ. 1986. Organic matter mineralization with reduction of ferric iron in anaerobic sediments. Appl. Environ. Microbiol. 51: 683-689.
53. Staudinger J, Roberts PV. 1996. A critical review of Henry's law constants for environmental applications. Crit. Rev. Environ. Sci. Technol. 26:205-297.
54. 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.
55. 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.
56. Caccavo F, Jr, Lonergan DJ, Lovley DR, Davis M, Stolz JF, McInerney MJ. 1994. Geobacter sulfurreducens sp. nov., a hydrogen-and acetateoxidizing dissimilatory metal-reducing microorganism. Appl. Environ. Microbiol. 60:3752-3759.
57. Egland PG, Gibson J, Harwood CS. 1995. Benzoate-coenzyme A ligase, encoded by badA, is one of three ligases able to catalyze benzoyl-coenzyme A formation during anaerobic growth of Rhodopseudomonas palustris on benzoate. J. Bacteriol. 177:6545-6551.
58. Schühle K, Gescher J, Feil U, Paul M, Jahn M, Schagger H, Fuchs G. 2003. Benzoate-coenzyme A ligase from Thauera aromatica: an enzyme acting in anaerobic and aerobic pathways. J. Bacteriol. 185:4920-4929.
59. Wischgoll S, Heintz D, Peters F, Erxleben A, Sarnighausen E, Reski R, Van Dorsselaer A, Boll M. 2005. Gene clusters involved in anaerobic benzoate degradation of Geobacter metallireducens. Mol. Microbiol. 58: 1238-1252.
60. Butler JE, He Q, Nevin KP, He Z, Zhou J, Lovley DR. 2007. Genomic and microarray analysis of aromatics degradation in Geobacter metallireducens and comparison to a Geobacter isolate from a contaminated field site. BMC Genomics 8:180. doi:10.1186/1471-2164-8-180.
61. Schmeling S, Narmandakh A, Schmitt O, Gad'on N, Schuhle K, Fuchs G. 2004. Phenylphosphate synthase: a new phosphotransferase catalyzing the first step in anaerobic phenol metabolism in Thauera aromatica. J. Bacteriol. 186:8044-8057.
62. Leuthner B, Leutwein C, Schulz H, Horth P, Haehnel W, Schiltz E, Schagger H, Heider J. 1998. Biochemical and genetic characterization of benzylsuccinate synthase from Thauera aromatica: a new glycyl radical enzyme catalysing the first step in anaerobic toluene metabolism. Mol. Microbiol. 28:615-628.
63. Peters F, Heintz D, Johannes J, van Dorsselaer A, Boll M. 2007. Genes, enzymes, and regulation of para-cresol metabolism in Geobacter metallireducens. J. Bacteriol. 189:4729-4738.
64. Schleinitz KM, Schmeling S, Jehmlich N, von Bergen M, Harms H, Kleinsteuber S, Vogt C, Fuchs G. 2009. Phenol degradation in the strictly anaerobic iron-reducing bacterium Geobacter metallireducens GS-15. Appl. Environ. Microbiol. 75:3912-3919.
65. Schuhle K, Fuchs G. 2004. Phenylphosphate carboxylase: a new C-C lyase involved in anaerobic phenol metabolism in Thauera aromatica. J. Bacteriol. 186:4556-4567.
66. Oberender J, Kung JW, Seifert J, von Bergen M, Boll M. 2012. Identification and characterization of a succinyl-coenzyme A (CoA):benzoate CoA transferase in Geobacter metallireducens. J. Bacteriol. 194:2501-2508.
67. 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.
68. 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.
69. 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.
70. Reguera G, McCarthy KD, Mehta T, Nicoll JS, Tuominen MT, Lovley DR. 2005. Extracellular electron transfer via microbial nanowires. Nature 435:1098-1101.
71. Smith JA, Lovley DR, Tremblay PL. 2013. Outer cell surface components essential for Fe(III) oxide reduction by Geobacter metallireducens. Appl. Environ. Microbiol. 79:901-907.