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Primers: Functional Genes for Aerobic Chlorinated Hydrocarbon-Degrading Microbes

Protocol
Part of the Springer Protocols Handbooks book series (SPH)

Abstract

Bioremediation offers a solution to the problem of chlorinated hydrocarbon pollution. Small chlorinated compounds can be mineralised by aerobic bacteria, acting as carbon and energy sources, and the genes that encode these processes can be detected and monitored by PCR. This provides a rapid, specific, culture-independent, and potentially quantitative tool of enormous utility to bioremediation practitioners. This chapter summarises and evaluates available PCR primers for genes encoding metabolism of organochlorines, especially chlorinated alkanes, alkenes, and alkanoic acids. The enzyme families involved include hydrolytic dehalogenases, dehydrochlorinases, monooxygenases, glutathione-S-transferases, and corrinoid-dependent enzymes. Although aromatic dioxygenases are important enzymes for degradation of chlorinated aromatic hydrocarbons, this enzyme family is not discussed here. This chapter assumes a basic knowledge of PCR and primer design. The focus will be on the design and use of degenerate primers and on the relationships between genes, bacteria, and chlorinated substrates.

Keywords:

Biodegradation Bioremediation Chloroalkane Chloroalkene Dechlorination Dehalogenase Halidohydrolase Monooxygenase Organochlorine qPCR 

References

  1. 1.
    Illman WA, Alvarez PJ (2009) Performance assessment of bioremediation and natural attenuation. Crit Rev Environ Sci Technol 39:209–270CrossRefGoogle Scholar
  2. 2.
    Lee MD, Odom JM, Buchanan RJJ (1998) New perspectives on microbial dehalogenation of chlorinated solvents: insights from the field. Annu Rev Microbiol 52:423–452PubMedCrossRefGoogle Scholar
  3. 3.
    Field JA, Sierra-Alvarez R (2008) Microbial transformation and degradation of polychlorinated biphenyls. Environ Pollut 155:1–12PubMedCrossRefGoogle Scholar
  4. 4.
    Aislabie JM, Richards NK, Boul HL (1997) Microbial degradation of DDT and its residues – a review. N Z J Agric Res 40:269–282CrossRefGoogle Scholar
  5. 5.
    Mattes TE, Alexander AK, Coleman NV (2010) Aerobic biodegradation of the chloroethenes: pathways, enzymes, ecology, and evolution. FEMS Microbiol Rev 34:445–475PubMedCrossRefGoogle Scholar
  6. 6.
    Janssen DB, Dinkla IJT, Poelarends GJ, Terpstra P (2005) Bacterial degradation of xenobiotic compounds: evolution and distribution of novel enzyme activities. Environ Microbiol 7:1868–1882PubMedCrossRefGoogle Scholar
  7. 7.
    McDonald IR, Warner KL, McAnulla C, Woodall CA, Oremland RS, Murrell JC (2002) A review of bacterial methyl halide degradation: biochemistry, genetics and molecular ecology. Environ Microbiol 4:193–203PubMedCrossRefGoogle Scholar
  8. 8.
    Pazmino DET, Winkler M, Glieder A, Fraaije MW (2010) Monooxygenases as biocatalysts: classification, mechanistic aspects and biotechnological applications. J Biotechnol 146:9–24CrossRefGoogle Scholar
  9. 9.
    Leak DJ, Sheldon RA, Woodley JM, Adlercreutz P (2009) Biocatalysts for selective introduction of oxygen. Biocatal Biotransform 27:1–26CrossRefGoogle Scholar
  10. 10.
    Leahy JG, Batchelor PJ, Morcomb SM (2003) Evolution of the soluble diiron monooxygenases. FEMS Microbiol Rev 27:449–479PubMedCrossRefGoogle Scholar
  11. 11.
    Lieberman RL, Rosenzweig AC (2004) Biological methane oxidation: regulation, biochemistry, and active site structure of particulate methane monooxygenase. Crit Rev Biochem Mol Biol 39:147–164PubMedCrossRefGoogle Scholar
  12. 12.
    Wackett LP (1995) Bacterial co-metabolism of halogenated organic compounds. In: Young LY, Cerniglia CE (eds) Microbial transformation and degradation of toxic organic chemicals. Wiley-Liss, New York, pp 217–241Google Scholar
  13. 13.
    Semprini L (1997) Strategies for the aerobic co-metabolism of chlorinated solvents. Curr Opin Biotechnol 8:296–308PubMedCrossRefGoogle Scholar
  14. 14.
    Holmes AJ, Coleman NV (2008) Evolutionary ecology and multidisciplinary approaches to prospecting for monooxygenases as biocatalysts. Anton Leeuw Int J Gen Mol Microbiol 94:75–84CrossRefGoogle Scholar
  15. 15.
    Coleman NV, Bui NB, Holmes AJ (2006) Soluble di-iron monooxygenase gene diversity in soils, sediments and ethene enrichments. Environ Microbiol 8:1228–1239PubMedCrossRefGoogle Scholar
  16. 16.
    Owens CR, Karceski JK, Mattes TE (2009) Gaseous alkene biotransformation and enantioselective epoxyalkane formation by Nocardioides sp. strain JS614. Appl Microbiol Biotechnol 84:685–692PubMedCrossRefGoogle Scholar
  17. 17.
    Rose TM, Schultz ER, Henikoff JG, Pietrokovski S, McCallum CM, Henikoff S (1998) Consensus-degenerate hybrid oligonucleotide primers for amplification of distantly related sequences. Nucleic Acids Res 26:1628–1635PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    ATSDR (1997) Toxicological profile for vinyl chloride. Update (final report). Atlanta, GA. NTIS Accession No. PB98-101132Google Scholar
  19. 19.
    Cunningham JJ, Kinner NE, Lewis M (2009) Protistan predation affects trichloroethene biodegradation in a bedrock aquifer. Appl Environ Microbiol 75:7588–7593PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Shim H, Ryoo D, Barbieri P, Wood TK (2001) Aerobic degradation of mixtures of tetrachloroethylene, trichloroethylene, dichloroethylenes, and vinyl chloride by toluene-o-xylene monooxygenase of Pseudomonas stutzeri OX1. Appl Microbiol Biotechnol 56:265–269PubMedCrossRefGoogle Scholar
  21. 21.
    Witt ME, Klecka GM, Lutz EJ, Ei TA, Grosso NR, Chapelle FH (2002) Natural attenuation of chlorinated solvents at Area 6, Dover Air Force Base: groundwater biogeochemistry. J Contam Hydrol 57:61–80PubMedCrossRefGoogle Scholar
  22. 22.
    Davis GB, Patterson BM, Johnston CD (2009) Aerobic bioremediation of 1,2 dichloroethane and vinyl chloride at field scale. J Contam Hydrol 107:91–100PubMedCrossRefGoogle Scholar
  23. 23.
    Bradley PM (2003) History and ecology of chloroethene biodegradation: a review. Biorem J 7:81–109CrossRefGoogle Scholar
  24. 24.
    Hartmans S, De Bont JA (1992) Aerobic vinyl chloride metabolism in Mycobacterium aurum L1. Appl Environ Microbiol 58:1220–1226PubMedPubMedCentralGoogle Scholar
  25. 25.
    Coleman NV, Spain JC (2003) Epoxyalkane:coenzyme M transferase in the ethene and vinyl chloride biodegradation pathways of Mycobacterium Strain JS60. J Bacteriol 185:5536–5545PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Chuang AS, Mattes TE (2007) Identification of polypeptides expressed in response to vinyl chloride, ethene, and epoxyethane in Nocardioides sp. strain JS614 by using peptide mass fingerprinting. Appl Environ Microbiol 73:4368–4372PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Jin YO, Mattes TE (2008) Adaptation of aerobic, ethene-assimilating Mycobacterium strains to vinyl chloride as a growth substrate. Environ Sci Technol 42:4784–4789PubMedCrossRefGoogle Scholar
  28. 28.
    Jin YO, Cheung S, Coleman NV, Mattes TE (2010) Association of missense mutations in epoxyalkane coenzyme M transferase with adaptation of Mycobacterium sp. strain JS623 to growth on vinyl chloride. Appl Environ Microbiol 76:3413–3419PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Coleman NV, Yau S, Wilson NL et al (2011) Untangling the multiple monooxygenases of Mycobacterium chubuense strain NBB4, a versatile hydrocarbon degrader. Environ Microbiol Rep 3:297–307PubMedCrossRefGoogle Scholar
  30. 30.
    Jin YO, Mattes TE (2010) A quantitative PCR assay for aerobic, vinyl chloride- and ethene-assimilating microorganisms in groundwater. Environ Sci Technol 44:9036–9041PubMedCrossRefGoogle Scholar
  31. 31.
    Suzuki T, Nakamura T, Fuse H (2012) Isolation of two novel marine ethylene-assimilating bacteria, Haliea species ETY-M and ETY-NAG, containing particulate methane monooxygenase-like genes. Microbes Environ 27:54–60PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Jin YO, Mattes TE (2011) Assessment and modification of degenerate qPCR primers that amplify functional genes from etheneotrophs and vinyl chloride-assimilators. Lett Appl Microbiol 53:576–580PubMedCrossRefGoogle Scholar
  33. 33.
    Dunaway JM (2002) Status of chemical alternatives to methyl bromide for pre-plant fumigation of soil. Phytopathology 92:1337–1343CrossRefGoogle Scholar
  34. 34.
    Cox MJ, Schaefer H, Nightingale PD, McDonald IR, Murrell JC (2012) Diversity of methyl halide-degrading microorganisms in oceanic and coastal waters. FEMS Microbiol Lett 334:111–118PubMedCrossRefGoogle Scholar
  35. 35.
    Woodall CA, Warner KL, Oremland RS, Murrell JC, McDonald IR (2001) Identification of methyl halide-utilizing genes in the methyl bromide-utilizing bacterial strain IMB-1 suggests a high degree of conservation of methyl halide-specific genes in gram-negative bacteria. Appl Environ Microbiol 67:1959–1963PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Vannelli T, Messmer M, Studer A, Vuilleumier S, Leisinger T (1999) A corrinoid-dependent catabolic pathway for growth of a Methylobacterium strain with chloromethane. Proc Natl Acad Sci U S A 96:4615–4620PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    McAnulla C, Woodall CA, McDonald IR et al (2001) Chloromethane utilization gene cluster from Hyphomicrobium chloromethanicum strain CM2(T) and development of functional gene probes to detect halomethane-degrading bacteria. Appl Environ Microbiol 67:307–316PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Miller LG, Warner KL, Baesman SM et al (2004) Degradation of methyl bromide and methyl chloride in soil microcosms: use of stable C isotope fractionation and stable isotope probing to identify reactions and the responsible microorganisms. Geochim Cosmochim Acta 68:3271–3283CrossRefGoogle Scholar
  39. 39.
    Borodina E, Cox MJ, McDonald IR, Murrell JC (2005) Use of DNA-stable isotope probing and functional gene probes to investigate the diversity of methyl chloride-utilizing bacteria in soil. Environ Microbiol 7:1318–1328PubMedCrossRefGoogle Scholar
  40. 40.
    Schafer H, McDonald IR, Nightingale PD, Murrell JC (2005) Evidence for the presence of a CmuA methyltransferase pathway in novel marine methyl halide-oxidizing bacteria. Environ Microbiol 7:839–852PubMedCrossRefGoogle Scholar
  41. 41.
    Nadalig T, Farhan U, Haque M, Roselli S, Schaller H, Bringel F, Vuilleumier S (2011) Detection and isolation of chloromethane-degrading bacteria from the Arabidopsis thaliana phyllosphere, and characterization of chloromethane utilization genes. FEMS Microbiol Ecol 77:438–448PubMedCrossRefGoogle Scholar
  42. 42.
    Moran MJ, Zogorski JS, Squillace PJ (2007) Chlorinated solvents in groundwater of the United States. Environ Sci Technol 41:74–81PubMedCrossRefGoogle Scholar
  43. 43.
    Bailon L, Nikolausz M, Kastner M, Veiga MC, Kennes C (2009) Removal of dichloromethane from waste gases in one- and two-liquid-phase stirred tank bioreactors and biotrickling filters. Water Res 43:11–20PubMedCrossRefGoogle Scholar
  44. 44.
    Firsova YE, Fedorov DN, Trotsenko YA (2011) Analysis of the 3′-region of the dcmA gene of dichloromethane dehalogenase of Methylobacterium dichloromethanicum DM4. Microbiology SGM 80:805–811CrossRefGoogle Scholar
  45. 45.
    Kayser MF, Ucurum Z, Vuilleumier S (2002) Dichloromethane metabolism and C-1 utilization genes in Methylobacterium strains. Microbiology SGM 148:1915–1922CrossRefGoogle Scholar
  46. 46.
    Muller EEL, Bringel F, Vuilleumier S (2011) Dichloromethane-degrading bacteria in the genomic age. Res Microbiol 162:869–876PubMedCrossRefGoogle Scholar
  47. 47.
    Vuilleumier S, Ivos N, Dean M, Leisinger T (2001) Sequence variation in dichloromethane dehalogenases/glutathione S-transferases. Microbiology 147:611–619PubMedCrossRefGoogle Scholar
  48. 48.
    Firsova JE, Doronina NV, Trotsenko YA (2010) Analysis of the key functional genes in new aerobic degraders of dichloromethane. Microbiology SGM 79:66–72CrossRefGoogle Scholar
  49. 49.
    Squillace PJ, Moran MJ, Lapham WW, Price CV, Clawges RM, Zogorski JS (1999) Volatile organic compounds in untreated ambient groundwater of the United States, 1985–1995. Environ Sci Technol 33:4176–4187CrossRefGoogle Scholar
  50. 50.
    Keuning S, Janssen DB, Witholt B (1985) Purification and characterization of hydrolytic haloalkane dehalogenase from Xanthobacter autotrophicus GJ10. J Bacteriol 163:635–639PubMedPubMedCentralGoogle Scholar
  51. 51.
    Janssen D, Pries F, Van der Ploeg J, Kazemier B, Terpstra P, Witholt B (1989) Cloning of 1,2-dichloroethane degradation genes of Xanthobacter autotrophicus GJ10 and expression and sequencing of the dhlA gene. J Bacteriol 171:6791–6799PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    van den Wijngaard AJ, van der Kamp KW, van der Ploeg J, Pries F, Kazemier B, Janssen DB (1992) Degradation of 1,2-dichloroethane by Ancylobacter aquaticus and other facultative methylotrophs. Appl Environ Microbiol 58:976–983PubMedPubMedCentralGoogle Scholar
  53. 53.
    Munro JE, Liew EF, Coleman NV (2013) Adaptation of a membrane bioreactor to 1,2-dichloroethane revealed by 16S rDNA pyrosequencing and dhlA qPCR. Environ Sci Technol 47:13668–13676PubMedCrossRefGoogle Scholar
  54. 54.
    Song JS, Lee DH, Lee K, Kim CK (2004) Genetic organization of the dhlA gene encoding 1,2-dichloroethane dechlorinase from Xanthobacter flavus UE15. J Microbiol 42:188–193PubMedGoogle Scholar
  55. 55.
    Hage JC, Hartmans S (1999) Monooxygenase-mediated 1,2-dichloroethane degradation by Pseudomonas sp. strain DCA1. Appl Environ Microbiol 65:2466–2470PubMedPubMedCentralGoogle Scholar
  56. 56.
    Nishino SF, Shin KA, Gossett JM, Spain JC (2013) Cytochrome p450 initiates degradation of cis-dichloroethene by Polaromonas sp. strain JS666. Appl Environ Microbiol 79:2263–2272PubMedPubMedCentralCrossRefGoogle Scholar
  57. 57.
    Olaniran AO, Naidoo S, Masango MG, Pillay B (2007) Aerobic biodegradation of 1,2-dichloroethane and 1,3-dichloropropene by bacteria isolated from a pulp mill wastewater effluent in South Africa. Biotechnol Bioprocess Eng 12:276–281CrossRefGoogle Scholar
  58. 58.
    Mileva A, Sapundzhiev T, Beschkov V (2008) Modeling 1,2-dichloroethane biodegradation by Klebsiella oxytoca va 8391 immobilized on granulated activated carbon. Bioprocess Biosyst Eng 31:75–85PubMedCrossRefGoogle Scholar
  59. 59.
    Dinglasan-Panlilio MJ, Dworatzek S, Mabury S, Edwards E (2006) Microbial oxidation of 1,2-dichloroethane under anoxic conditions with nitrate as electron acceptor in mixed and pure cultures. FEMS Microbiol Ecol 56:355–364PubMedCrossRefGoogle Scholar
  60. 60.
    Koudelakova T, Bidmanova S, Dvorak P et al (2013) Haloalkane dehalogenases: biotechnological applications. Biotechnol J 8:32–45PubMedCrossRefGoogle Scholar
  61. 61.
    Carr PD, Ollis DL (2009) Alpha/beta hydrolase fold: an update. Protein Pept Lett 16:1137–1148PubMedCrossRefGoogle Scholar
  62. 62.
    Kotik M, Famerova V (2012) Sequence diversity in haloalkane dehalogenases, as revealed by PCR using family-specific primers. J Microbiol Methods 88:212–217PubMedCrossRefGoogle Scholar
  63. 63.
    Tardif G, Greer CW, Labbe D, Lau PC (1991) Involvement of a large plasmid in the degradation of 1,2-dichloroethane by Xanthobacter autotrophicus. Appl Environ Microbiol 57:1853–1857PubMedPubMedCentralGoogle Scholar
  64. 64.
    Govender A, Shaik R, Abbai NS, Pillay B (2011) Dehalogenase gene detection and microbial diversity of a chlorinated hydrocarbon contaminated site. World J Microbiol Biotechnol 27:2407–2414CrossRefGoogle Scholar
  65. 65.
    Stucki G, Thuer M (1995) Experiences of a large scale application of 1,2-dichloroethane degrading microorganisms for groundwater treatment. Environ Sci Technol 29:2339–2345PubMedCrossRefGoogle Scholar
  66. 66.
    Poelarends GJ, Zandstra M, Bosma T et al (2000) Haloalkane-utilizing Rhodococcus strains isolated from geographically distinct locations possess a highly conserved gene cluster encoding haloalkane catabolism. J Bacteriol 182:2725–2731PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    Poelarends GJ, Wilkens M, Larkin MJ, van Elsas JD, Janssen DB (1998) Degradation of 1,3-dichloropropene by Pseudomonas cichorii 170. Appl Environ Microbiol 64:2931–2936PubMedPubMedCentralGoogle Scholar
  68. 68.
    Poelarends GJ, Kulakov LA, Larkin MJ, van Hylckama Vlieg JET, Janssen DB (2000) Roles of horizontal gene transfer and gene integration in evolution of 1,3-dichloropropene-and 1,2-dibromoethane-degradative pathways. J Bacteriol 182:2191–2199PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    Lal R, Pandey G, Sharma P, Kumari K, Malhotra S, Pandey R, Raina V, Kohler HP, Holliger C, Jackson C, Oakeshott JG (2010) Biochemistry of microbial degradation of hexachlorocyclohexane and prospects for bioremediation. Microbiol Mol Biol Rev 74:58–80PubMedPubMedCentralCrossRefGoogle Scholar
  70. 70.
    Lal R, Dogra C, Malhotra S, Sharma P, Pal R (2006) Diversity, distribution and divergence of lin genes in hexachlorocyclohexane-degrading sphingomonads. Trends Biotechnol 24:121–130PubMedCrossRefGoogle Scholar
  71. 71.
    Kuramochi N, Otsuka S, Nishiyama M, Senoo K (2007) Presence of linA-homologous DNA sequences in different types of soil and their sequence diversity. Microbes Environ 22:399–404CrossRefGoogle Scholar
  72. 72.
    Yamamoto S, Otsuka S, Murakami Y, Nishiyama M, Senoo K (2009) Genetic diversity of gamma-hexachlorocyclohexane-degrading sphingomonads isolated from a single experimental field. Lett Appl Microbiol 49:472–477PubMedCrossRefGoogle Scholar
  73. 73.
    Sharma P, Jindal S, Bala K et al (2014) Functional screening of enzymes and bacteria for the dechlorination of hexachlorocyclohexane by a high-throughput colorimetric assay. Biodegradation 25:179–187PubMedCrossRefGoogle Scholar
  74. 74.
    Gupta SK, Lal D, Lata P et al (2013) Changes in the bacterial community and lin genes diversity during biostimulation of indigenous bacterial community of hexachlorocyclohexane (HCH) dumpsite soil. Microbiology SGM 82:234–240CrossRefGoogle Scholar
  75. 75.
    Manickam N, Pathak A, Saini HS, Mayilraj S, Shanker R (2010) Metabolic profiles and phylogenetic diversity of microbial communities from chlorinated pesticides contaminated sites of different geographical habitats of India. J Appl Microbiol 109:1458–1468PubMedCrossRefGoogle Scholar
  76. 76.
    Fuchu G, Ohtsubo Y, Ito M et al (2008) Insertion sequence-based cassette PCR: cultivation-independent isolation of gamma-hexachlorocyclohexane-degrading genes from soil DNA. Appl Microbiol Biotechnol 79:627–632PubMedCrossRefGoogle Scholar
  77. 77.
    Dogra C, Raina V, Pal R, Suar M, Lal S, Gartemann KH, Holliger C, van der Meer JR, Lal R (2004) Organization of lin genes and IS6100 among different strains of hexachlorocyclohexane-degrading Sphingomonas paucimobilis: evidence for horizontal gene transfer. J Bacteriol 186:2225–2235PubMedPubMedCentralCrossRefGoogle Scholar
  78. 78.
    Gribble GW (1992) Naturally-occurring organohalogen compounds – a survey. J Nat Prod 55:1353–1395CrossRefGoogle Scholar
  79. 79.
    Khosrowabadi E, Huyop F (2014) Screening and characterization of several 2,2-dichloropropionic acid-degrading bacteria isolated from marine sediment of Danga Bay and east coast of Singapore island. Biorem J 18:20–27CrossRefGoogle Scholar
  80. 80.
    Hill KE, Marchesi JR, Weightman AJ (1999) Investigation of two evolutionarily unrelated halocarboxylic acid dehalogenase gene families. J Bacteriol 181:2535–2547PubMedPubMedCentralGoogle Scholar
  81. 81.
    Marchesi JR, Weightman AJ (2003) Diversity of alpha-halocarboxylic acid dehalogenases in bacteria isolated from a pristine soil after enrichment and selection on the herbicide 2,2-dichloropropionic acid (Dalapon). Environ Microbiol 5:48–54PubMedCrossRefGoogle Scholar
  82. 82.
    Marchesi JR, Weightman AJ (2003) Comparing the dehalogenase gene pool in cultivated alpha-halocarboxylic acid-degrading bacteria with the environmental metagene pool. Appl Environ Microbiol 69:4375–4382PubMedPubMedCentralCrossRefGoogle Scholar
  83. 83.
    Ferrari BC, Binnerup SJ, Gillings M (2005) Microcolony cultivation on a soil substrate membrane system selects for previously uncultured soil bacteria. Appl Environ Microbiol 71:8714–8720PubMedPubMedCentralCrossRefGoogle Scholar
  84. 84.
    Connon SA, Giovannoni SJ (2002) High-throughput methods for culturing microorganisms in very-low-nutrient media yield diverse new marine isolates. Appl Environ Microbiol 68:3878–3885PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Leach LH, Zhang P, LaPara TM, Hozalski RM, Camper AK (2009) Detection and enumeration of haloacetic acid-degrading bacteria in drinking water distribution systems using dehalogenase genes. J Appl Microbiol 107:978–988PubMedCrossRefGoogle Scholar
  86. 86.
    Grigorescu AS, Hozalski RM, LaPara TM (2012) Haloacetic acid-degrading bacterial communities in drinking water systems as determined by cultivation and by terminal restriction fragment length polymorphism of PCR-amplified haloacid dehalogenase gene fragments. J Appl Microbiol 112:809–822PubMedCrossRefGoogle Scholar
  87. 87.
    Baek K, McKeever R, Rieber K et al (2012) Molecular approach to evaluate biostimulation of 1,2-dibromoethane in contaminated groundwater. Bioresour Technol 123:207–213PubMedCrossRefGoogle Scholar
  88. 88.
    van der Ploeg J, van Hall G, Janssen DB (1991) Characterization of the haloacid dehalogenase from Xanthobacter autotrophicus GJ10 and sequencing of the dhlB gene. J Bacteriol 173:7925–7933PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    Weightman AJ, Slater JH, Bull AT (1979) Partial purification of two dehalogenases from Pseudomonas putida Pp3. FEMS Microbiol Lett 6:231–234CrossRefGoogle Scholar
  90. 90.
    Fortin N, Fulthorpe RR, Allen DG, Greer CW (1998) Molecular analysis of bacterial isolates and total community DNA from kraft pulp mill effluent treatment systems. Can J Microbiol 44:537–546PubMedCrossRefGoogle Scholar
  91. 91.
    Mattes TE, Alexander AK, Richardson PM et al (2008) The genome of Polaromonas sp. strain JS666: insights into the evolution of a hydrocarbon- and xenobiotic-degrading bacterium, and features of relevance to biotechnology. Appl Environ Microbiol 74:6405–6416PubMedPubMedCentralCrossRefGoogle Scholar
  92. 92.
    Coleman NV, Mattes TE, Gossett JM, Spain JC (2002) Biodegradation of cis-dichloroethene as the sole carbon source by a beta-proteobacterium. Appl Environ Microbiol 68:2726–2730PubMedPubMedCentralCrossRefGoogle Scholar
  93. 93.
    Gintautas PA, Daniel SR, Macalady DL (1992) Phenoxyalkanoic acid herbicides in municipal landfill leachates. Environ Sci Technol 26:517–521CrossRefGoogle Scholar
  94. 94.
    Dunbar J, White S, Forney L (1997) Genetic diversity through the looking glass: effect of enrichment bias. Appl Environ Microbiol 63:1326–1331PubMedPubMedCentralGoogle Scholar
  95. 95.
    Fukumori F, Hausinger RP (1993) Alcaligenes eutrophus JMP134 2,4-dichlorophenoxyacetate monooxygenase is an alpha-ketoglutarate-dependent dioxygenase. J Bacteriol 175:2083–2086PubMedPubMedCentralCrossRefGoogle Scholar
  96. 96.
    Ka JO, Holben WE, Tiedje JM (1994) Genetic and phenotypic diversity of 2,4-dichlorophenoxyacetic acid (2,4-D)-degrading bacteria isolated from 2,4-D-treated field soils. Appl Environ Microbiol 60:1106–1115PubMedPubMedCentralGoogle Scholar
  97. 97.
    Kitagawa W, Takami S, Miyauchi K et al (2002) Novel 2,4-dichlorophenoxyacetic acid degradation genes from oligotrophic Bradyrhizobium sp. strain HW13 isolated from a pristine environment. J Bacteriol 184:509–518PubMedPubMedCentralCrossRefGoogle Scholar
  98. 98.
    Wright TR, Shan G, Walsh TA, Lira JM, Cui C, Song P, Zhuang M, Arnold NL, Lin G, Yau K, Russell SM, Cicchillo RM, Peterson MA, Simpson DM, Zhou N, Ponsamuel J, Zhang Z (2010) Robust crop resistance to broadleaf and grass herbicides provided by aryloxyalkanoate dioxygenase transgenes. Proc Natl Acad Sci U S A 107:20240–20245PubMedPubMedCentralCrossRefGoogle Scholar
  99. 99.
    Vallaeys T, Fulthorpe RR, Wright AM, Soulas G (1996) The metabolic pathway of 2,4-dichlorophenoxyacetic acid degradation involves different families of tfdA and tfdB genes according to PCR-RFLP analysis. FEMS Microbiol Ecol 20:163–172CrossRefGoogle Scholar
  100. 100.
    Lillis L, Clipson N, Doyle E (2010) Quantification of catechol dioxygenase gene expression in soil during degradation of 2,4-dichlorophenol. FEMS Microbiol Ecol 73:363–369PubMedGoogle Scholar
  101. 101.
    Shaw LJ, Burns RG (2004) Enhanced mineralization of [U-(14)C] 2,4-dichlorophenoxyacetic acid in soil from the rhizosphere of Trifolium pratense. Appl Environ Microbiol 70:4766–4774PubMedPubMedCentralCrossRefGoogle Scholar
  102. 102.
    Gazitua MC, Slater AW, Melo F, Gonzalez B (2010) Novel alpha-ketoglutarate dioxygenase tfdA-related genes are found in soil DNA after exposure to phenoxyalkanoic herbicides. Environ Microbiol 12:2411–2425PubMedCrossRefGoogle Scholar
  103. 103.
    Zakaria D, Lappin-Scott H, Burton S, Whitby C (2007) Bacterial diversity in soil enrichment cultures amended with 2 (2-methyl-4-chlorophenoxy) propionic acid (mecoprop). Environ Microbiol 9:2575–2587PubMedCrossRefGoogle Scholar
  104. 104.
    Gonod LV, Martin-Laurent F, Chenu C (2006) 2,4-D impact on bacterial communities, and the activity and genetic potential of 2,4-D degrading communities in soil. FEMS Microbiol Ecol 58:529–537PubMedCrossRefGoogle Scholar
  105. 105.
    Baelum J, Henriksen T, Hansen HCB, Jacobsen CS (2006) Degradation of 4-chloro-2-methylphenoxyacetic acid in top- and subsoil is quantitatively linked to the class III tfdA gene. Appl Environ Microbiol 72:1476–1486PubMedPubMedCentralCrossRefGoogle Scholar
  106. 106.
    Baelum J, Nicolaisen MH, Holben WE, Strobel BW, Sorensen J, Jacobsen CS (2008) Direct analysis of tfdA gene expression by indigenous bacteria in phenoxy acid amended agricultural soil. ISME J 2:677–687PubMedCrossRefGoogle Scholar
  107. 107.
    Baelum J, Prestat E, David MM, Strobel BW, Jacobsen CS (2012) Modeling of phenoxy acid herbicide mineralization and growth of microbial degraders in 15 Soils monitored by quantitative real-time PCR of the functional tfdA gene. Appl Environ Microbiol 78:5305–5312PubMedPubMedCentralCrossRefGoogle Scholar
  108. 108.
    Baelum J, Jacobsen CS (2009) TaqMan probe-based real-Time PCR assay for detection and discrimination of class I, II, and III tfdA genes in soils treated with phenoxy acid herbicides. Appl Environ Microbiol 75:2969–2972PubMedPubMedCentralCrossRefGoogle Scholar
  109. 109.
    Zaprasis A, Liu Y-J, Liu S-J, Drake HL, Horn MA (2010) Abundance of novel and diverse tfdA-like genes, encoding putative phenoxyalkanoic acid herbicide-degrading dioxygenases, in soil. Appl Environ Microbiol 76:119–128PubMedCrossRefGoogle Scholar
  110. 110.
    Paulin MM, Nicolaisen MH, Sorensen J (2010) Abundance and expression of enantioselective rdpA and sdpA dioxygenase genes during degradation of the racemic herbicide (R, S)-2-(2,4-dichlorophenoxy)propionate in soil. Appl Environ Microbiol 76:2873–2883PubMedPubMedCentralCrossRefGoogle Scholar
  111. 111.
    de Souza ML, Seffernick J, Martinez B, Sadowsky MJ, Wackett LP (1998) The atrazine catabolism genes atzABC are widespread and highly conserved. J Bacteriol 180:1951–1954PubMedPubMedCentralGoogle Scholar
  112. 112.
    Arbeli Z, Fuentes C (2010) Prevalence of the gene trzN and biogeographic patterns among atrazine-degrading bacteria isolated from 13 Colombian agricultural soils. FEMS Microbiol Ecol 73:611–623PubMedGoogle Scholar
  113. 113.
    De Souza ML, Newcombe D, Alvey S et al (1998) Molecular basis of a bacterial consortium: interspecies catabolism of atrazine. Appl Environ Microbiol 64:178–184PubMedPubMedCentralGoogle Scholar
  114. 114.
    Sajjaphan K, Shapir N, Wackett LP et al (2004) Arthrobacter aurescens TC1 atrazine catabolism genes trzN, atzB, and atzC are linked on a 160-kilobase region and are functional in Escherichia coli. Appl Environ Microbiol 70:4402–4407PubMedPubMedCentralCrossRefGoogle Scholar
  115. 115.
    Udikovic-Kolic N, Scott C, Martin-Laurent F (2012) Evolution of atrazine-degrading capabilities in the environment. Appl Microbiol Biotechnol 96:1175–1189PubMedCrossRefGoogle Scholar
  116. 116.
    Martinez B, Tomkins J, Wackett LP, Wing R, Sadowsky MJ (2001) Complete nucleotide sequence and organization of the atrazine catabolic plasmid pADP-1 from Pseudomonas sp. strain ADP. J Bacteriol 183:5684–5697PubMedPubMedCentralCrossRefGoogle Scholar
  117. 117.
    Nagy I, Compernolle F, Ghys K, Vanderleyden J, Demot R (1995) A single cytochrome p-450 system is involved in degradation of the herbicides EPTC (s-ethyl dipropylthiocarbamate) and atrazine by Rhodococcus sp. strain NI86/21. Appl Environ Microbiol 61:2056–2060PubMedPubMedCentralGoogle Scholar
  118. 118.
    Smith D, Alvey S, Crowley DE (2005) Cooperative catabolic pathways within an atrazine-degrading enrichment culture isolated from soil. FEMS Microbiol Ecol 53:265–273PubMedCrossRefGoogle Scholar
  119. 119.
    Shapir N, Goux S, Mandelbaum RT, Pussemier L (2000) The potential of soil microorganisms to mineralize atrazine as predicted by MCH-PCR followed by nested PCR. Can J Microbiol 46:425–432PubMedCrossRefGoogle Scholar
  120. 120.
    Sherchan SP, Bachoon DS (2011) The presence of atrazine and atrazine-degrading bacteria in the residential, cattle farming, forested and golf course regions of Lake Oconee. J Appl Microbiol 111:293–299PubMedCrossRefGoogle Scholar
  121. 121.
    Devers M, Soulas G, Martin-Laurent F (2004) Real-time reverse transcription PCR analysis of expression of atrazine catabolism genes in two bacterial strains isolated from soil. J Microbiol Methods 56:3–15PubMedCrossRefGoogle Scholar
  122. 122.
    Martin-Laurent F, Cornet L, Ranjard L et al (2004) Estimation of atrazine-degrading genetic potential and activity in three French agricultural soils. FEMS Microbiol Ecol 48:425–435PubMedCrossRefGoogle Scholar
  123. 123.
    Monard C, Martin-Laurent F, Devers-Lamrani M, Lima O, Vandenkoornhuyse P, Binet F (2010) atz gene expressions during atrazine degradation in the soil drilosphere. Mol Ecol 19:749–759PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.School of Molecular BioscienceUniversity of SydneyDarlingtonAustralia

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