Metagenomics reveals diversity and abundance of meta-cleavage pathways in microbial communities from soil highly contaminated with jet fuel under air-sparging bioremediation

Environmental Microbiology

Volumn 11, Issue 9, 2009, Pages 2216-2227

  Brennerova, Maria V ^a   Josefiova, Jirina ^a   Brenner, Vladimir ^a   Pieper, Dietmar H ^b   Junca, Howard ^b,c  

^a INSTITUTE OF MICROBIOLOGY   (Czech Republic)

^b HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^c Genomics and Evolution of Communities of Environmental Microorganisms   (Colombia)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; CATECHOL 2,3 DIOXYGENASE; EXTRADIOL DIOXYGENASE; HYDROCARBON; OXYGENASE; PETROLEUM;

ARTICLE; BACTERIAL GENE; BACTERIUM; BIOREMEDIATION; ENVIRONMENTAL MONITORING; ENZYMOLOGY; GENETIC VARIABILITY; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; SOIL POLLUTANT;

BACTERIA; BASE SEQUENCE; BIODEGRADATION, ENVIRONMENTAL; CATECHOL 2,3-DIOXYGENASE; DNA, BACTERIAL; ENVIRONMENTAL MONITORING; GENES, BACTERIAL; GENETIC VARIATION; HYDROCARBONS; MOLECULAR SEQUENCE DATA; OXYGENASES; PETROLEUM; PHYLOGENY; SOIL MICROBIOLOGY; SOIL POLLUTANTS;

BURKHOLDERIA; BURKHOLDERIA SP.; ESCHERICHIA COLI; PSEUDOMONAS; PSEUDOMONAS PUTIDA; PSEUDOMONAS SP.; RALSTONIA PICKETTII;

EID: 69949104495     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2009.01943.x     Document Type: Article

References (54)

1. Andujar, E. Santero, E. (2003) Site-directed mutagenesis of an extradiol dioxygenase involved in tetralin biodegradation identifies residues important for activity or substrate specificity. Microbiology 149 : 1559 1567.
2. Andujar, E., Hernaez, M.J., Kaschabek, S.R., Reineke, W. Santero, E. (2000) Identification of an extradiol dioxygenase involved in tetralin biodegradation: gene sequence analysis and purification and characterization of the gene product. J Bacteriol 182 : 789 795.
3. Beil, S., Timmis, K.N. Pieper, D.H. (1999) Genetic and biochemical analyses of the tec operon suggest a route for evolution of chlorobenzene degradation genes. J Bacteriol 181 : 341 346.
4. Beloqui, A., Pita, M., Polaina, J., Martinez-Arias, A., Golyshina, O.V., Zumarraga, M., et al. (2006) Novel polyphenol oxidase mined from a metagenome expression library of bovine rumen: biochemical properties, structural analysis, and phylogenetic relationships. J Biol Chem 281 : 22933 22942.
5. Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of protein utilizing the principle of protein-dye binding. Anal Biochem 72 : 248 254.
6. Chablain, P.A., Zgoda, A.L., Sarde, C.O. Truffaut, N. (2001) Genetic and molecular organization of the alkylbenzene catabolism operon in the psychrotrophic strain Pseudomonas putida 01G3. Appl Environ Microbiol 67 : 453 458.
7. Di Gregorio, S., Zocca, C., Sidler, S., Toffanin, A., Lizzari, D. Vallini, G. (2004) Identification of two new sets of genes for dibenzothiophene transformation in Burkholderia sp. DBT1. Biodegradation 15 : 111 123.
8. Diaz, E., Ferrandez, A., Prieto, M.A. Garcia, J.L. (2001) Biodegradation of aromatic compounds by Escherichia coli. Microbiol Mol Biol Rev 65 : 523 569.
9. Dunwell, J.M., Khuri, S. Gane, P.J. (2000) Microbial relatives of the seed storage proteins of higher plants: conservation of structure and diversification of function during evolution of the cupin superfamily. Microbiol Mol Biol Rev 64 : 153 179.
10. Eaton, R.W. Timmis, K.N. (1986) Characterization of a plasmid-specified pathway for catabolism of isopropylbenzene in Pseudomonas putida RE204. J Bacteriol 168 : 123 131.
11. Eltis, L.D. Bolin, J.T. (1996) Evolutionary relationships among extradiol dioxygenases. J Bacteriol 178 : 5930 5937.
12. Ferrer, M., Golyshina, O.V., Chernikova, T.N., Khachane, A.N., Reyes-Duarte, D., Santos, V.A., et al. (2005) Novel hydrolase diversity retrieved from a metagenome library of bovine rumen microflora. Environ Microbiol 7 : 1996 2010.
13. Gibson, D.T. Parales, R.E. (2000) Aromatic hydrocarbon dioxygenases in environmental biotechnology. Curr Opin Biotechnol 11 : 236 243.
14. Gobel, M., Kranz, O.H., Kaschabek, S.R., Schmidt, E., Pieper, D.H. Reineke, W. (2004) Microorganisms degrading chlorobenzene via a meta-cleavage pathway harbor highly similar chlorocatechol 2,3-dioxygenase-encoding gene clusters. Arch Microbiol 182 : 147 156.
15. Habe, H., Kimura, T., Nojiri, H., Yamane, H. Omori, T. (1996) Cloning and nucleotide sequences of the genes involved in the meta-cleavage pathway of cumene degradation in Pseudomonas fluorescens IP01. J Ferment Bioeng 81 : 247 254.
16. Harayama, S., Mermod, N., Rekik, M., Lehrbach, P.R. Timmis, K.N. (1987) Roles of the divergent branches of the meta-cleavage pathway in the degradation of benzoate and substituted benzoates. J Bacteriol 169 : 558 564.
17. Harwood, C.S. Parales, R.E. (1996) The beta-ketoadipate pathway and the biology of self-identity. Annu Rev Microbiol 50 : 553 590.
18. Hatta, T., Mukerjee-Dhar, G., Damborsky, J., Kiyohara, H. Kimbara, K. (2003) Characterization of a novel thermostable Mn(II)-dependent 2,3-dihydroxybiphenyl 1,2-dioxygenase from a polychlorinated biphenyl- and naphthalene-degrading Bacillus sp. JF8. J Biol Chem 278 : 21483 21492.
19. Heiss, G., Stolz, A., Kuhm, A.E., Müller, C., Klein, J., Altenbuchner, J. Knackmuss, H.-J. (1995) Characterization of a 2,3-dihydroxybiphenyl dioxygenase from the naphthalenesulfonate-degrading bacterium strain BN6. J Bacteriol 177 : 5865 5871.
20. Hirose, J., Kimura, N., Suyama, A., Kobayashi, A., Hayashida, S. Furukawa, K. (1994) Functional and structural relationship of various extradiol aromatic ring-cleavage dioxygenases of Pseudomonas origin. FEMS Microbiol Lett 118 : 273 277. (Pubitemid 124012151)
21. Hofer, B., Backhaus, S. Timmis, K.N. (1994) The biphenyl/poychlorinated biphenyl-degradation locus (bph) of Pseudomonas sp. LB400 encodes four additional metabolic enzymes. Gene 144 : 9 16.
22. Iida, T., Nakamura, K., Izumi, A., Mukouzaka, Y. Kudo, T. (2006) Isolation and characterization of a gene cluster for dibenzofuran degradation in a new dibenzofuran-utilizing bacterium, Paenibacillus sp. strain YK5. Arch Microbiol 184 : 305 315.
23. Jeong, J.J., Kim, J.H., Kim, C.K., Hwang, I. Lee, K. (2003) 3- and 4-Alkylphenol degradation pathway in Pseudomonas sp. strain KL28: genetic organization of the lap gene cluster and substrate specificities of phenol hydroxylase and catechol 2,3-dioxygenase. Microbiology 149 : 3265 3277.
24. Junca, H., Plumeier, I., Hecht, H.J. Pieper, D.H. (2004) Difference in kinetic behaviour of catechol 2,3-dioxygenase variants from a polluted environment. Microbiology 150 : 4181 4187.
25. Kabelitz, N., Macháčkova, J., Imfeld, G., Brennerova, M., Přeper, D.H., Heipieper, H.J. Junca, H. (2009) Enhancement of the microbial community biomass and diversity during air sparging bioremediation of a soil highly contaminated with kerosene and BTEX. Appl Microbiol Biotechnol 82 : 565 577.
26. Kasuga, I., Nakajima, F. Furumai, H. (2007) Diversity of catechol 2,3-dioxygenase genes of bacteria responding to dissolved organic matter derived from different sources in a eutrophic lake. FEMS Microbiol Ecol 61 : 449 458.
27. Keil, H., Lebens, M.R. Williams, P.A. (1985) TOL plasmid pWW15 contains two nonhomologous, independently regulated catechol 2,3-oxygenase genes. J Bacteriol 163 : 248 255.
28. Kuhm, A.E., Stolz, A., Ngai, K.L. Knackmuss, H.J. (1991a) Purification and characterization of a 1,2-dihydroxynaphthalene dioxygenase from a bacterium that degrades naphthalenesulfonic acids. J Bacteriol 173 : 3795 3802.
29. Kuhm, A.E., Stolz, A. Knackmuss, H.-J. (1991b) Metabolism of naphthalene by the biphenyl-degrading bacterium Pseudomonas paucimobilis Q1. Biodegradation 2 : 115 120.
30. Kukor, J.J. Olsen, R.H. (1991) Genetic organization and regulation of a meta cleavage pathway for catechols produced from catabolism of toluene, benzene, phenol, and cresols by Pseudomonas pickettii PKO1. J Bacteriol 173 : 4587 4594.
31. Kukor, J.J. Olsen, R.H. (1996) Catechol 2,3-dioxygenases functional in oxygen-limited (hypoxic) environments. Appl Environ Microbiol 62 : 1728 1740.
32. Laurie, A.D. LloydJones, G. (1999) Conserved and hybrid meta-cleavage operons from PAH-degrading Burkholderia RP007. Biochem Biophys Res Commun 262 : 308 314.
33. Leahy, J.G., Batchelor, P.J. Morcomb, S.M. (2003) Evolution of the soluble diiron monooxygenases. FEMS Microbiol Rev 27 : 449 479.
34. Machackova, J., Wittlingerova, Z., Vlk, K., Zima, J. Linka, A. (2008) Comparison of two methods for assessment of in situ jet-fuel remediation efficiency. Water Air Soil Pollut 187 : 181 194.
35. McKay, D.B., Prucha, M., Reineke, W., Timmis, K.N. Pieper, D.H. (2003) Substrate specificity and expression of three 2,3-dihydroxybiphenyl 1,2-dioxygenases from Rhodococcus globerulus strain P6. J Bacteriol 185 : 2944 2951.
36. Margesin, R., Labbe, D., Schinner, F., Greer, C.W. Whyte, L.G. (2003) Characterization of hydrocarbon-degrading microbial populations in contaminated and pristine alpine soils. Appl Environ Microbiol 69 : 3085 3092.
37. Monferran, M.V., Echenique, J.R. Wunderlin, D.A. (2005) Degradation of chlorobenzenes by a strain of Acidovorax avenae isolated from a polluted aquifer. Chemosphere 61 : 98 106.
38. Moonen, M.J., Synowsky, S.A., van den Berg, W.A., Westphal, A.H., Heck, A.J., van den Heuvel, R.H., et al. (2008) Hydroquinone dioxygenase from Pseudomonas fluorescens ACB: a novel member of the family of nonheme-iron(II)-dependent dioxygenases. J Bacteriol 190 : 5199 5209.
39. Nogales, J., Canales, A., Jimenez-Barbero, J., Garcia, J.L. Diaz, E. (2005) Molecular characterization of the gallate dioxygenase from Pseudomonas putida KT2440. The prototype of a new subgroup of extradiol dioxygenases. J Biol Chem 280 : 35382 35390.
40. Pflugmacher, U., Averhoff, B. Gottschalk, G. (1996) Cloning, sequencing, and expression of isopropylbenzene degradation genes from Pseudomonas sp. strain JR1: identification of isopropylbenzene dioxygenase that mediates trichloroethene oxidation. Appl Environ Microbiol 62 : 3967 3977.
41. Pieper, D.H. (2005) Aerobic degradation of polychlorinated biphenyls. Appl Microbiol Biotechnol 67 : 170 191.
42. Riesenfeld, C.S., Goodman, R.M. Handelsman, J. (2004) Uncultured soil bacteria are a reservoir of new antibiotic resistance genes. Environ Microbiol 6 : 981 989.
43. Saitou, N. Nei, M. (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4 : 4606 4425.
44. Sambrook, J., Fritsch, E.F. Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY, USA : Cold Spring Harbor Laboratory Press.
45. Sei, K., Asano, K., Tateishi, N., Mori, K., Ike, M. Fujita, M. (1999) Design of PCR primers and gene probes for the general detection of bacterial populations capable of degrading aromatic compounds via catechol cleavage pathways. J Biosci Bioeng 88 : 542 550.
46. Selenska-Pobell, S., Kampf, G., Hemming, K., Radeva, G. Satchanska, G. (2001) Bacterial diversity in soil samples from two uranium waste piles as determined by rep-APD, RISA and 16S rDNA retrieval. Antonie Van Leeuwenhoek 79 : 149 161.
47. Shinoda, Y., Sakai, Y., Uenishi, H., Uchihashi, Y., Hiraishi, A., Yukawa, H., et al. (2004) Aerobic and anaerobic toluene degradation by a newly isolated denitrifying bacterium, Thauera sp. strain DNT-1. Appl Environ Microbiol 70 : 1385 1392.
48. Sipila, T.P., Riisio, H. Yrjala, K. (2006) Novel upper meta-pathway extradiol dioxygenase gene diversity in polluted soil. FEMS Microbiol Ecol 58 : 134 144.
49. Suenaga, H., Ohnuki, T. Miyazaki, K. (2007) Functional screening of a metagenomic library for genes involved in microbial degradation of aromatic compounds. Environ Microbiol 9 : 2289 2297.
50. Sugimoto, K., Senda, T., Aoshima, H., Masai, E., Fukuda, M. Mitsui, Y. (1999) Crystal structure of an aromatic ring opening dioxygenase LigAB, a protocatechuate 4,5-dioxygenase, under aerobic conditions. Structure 7 : 953 965.
51. Tamura, K., Dudley, J., Nei, M. Kumar, S. (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24 : 1596 1599.
52. Vaillancourt, F.H., Labbe, G., Drouin, N.M., Fortin, P.D. Eltis, L.D. (2002) The mechanism-based inactivation of 2,3-dihydroxybiphenyl 1,2-dioxygenase by catecholic substrates. J Biol Chem 277 : 2019 2027.
53. Witzig, R., Junca, H., Hecht, H.J. Pieper, D.H. (2006) Assessment of toluene/biphenyl dioxygenase gene diversity in benzene-polluted soils: links between benzene biodegradation and genes similar to those encoding isopropylbenzene dioxygenases. Appl Environ Microbiol 72 : 3504 3514.
54. Yeates, C., Holmes, A.J. Gillings, M.R. (2000) Novel forms of ring-hydroxylating dioxygenases are widespread in pristine and contaminated soils. Environ Microbiol 2 : 644 653.