Microbial dioxygenase gene population shifts during polycyclic aromatic hydrocarbon biodegradation

Applied and Environmental Microbiology

Volumn 72, Issue 6, 2006, Pages 4078-4087

  Chadhain, Sinéad M Ní ^a   Norman, R Sean ^a   Pesce, Karen V ^a   Kukor, Jerome J ^a,b   Zylstra, Gerben J ^a  

^a RUTGERS UNIVERSITY   (United States)

^b RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MICROBIAL DIOXYGENASE GENE POPULATION SHIFTS; POLYCYCLIC AROMATIC HYDROCARBON BIODEGRADATION; RIESKE IRON SULFUR;

BIODEGRADATION; ELECTROPHORESIS; ENZYME KINETICS; POLYCYCLIC AROMATIC HYDROCARBONS; RNA; SULFUR;

GENES;

DIOXYGENASE; IRON SULFUR PROTEIN; NAPHTHALENE; PHENANTHRENE; POLYCYCLIC AROMATIC HYDROCARBON; PYRENE; RIBOSOME RNA;

BIOASSAY; BIODEGRADATION; BIOMONITORING; BIOREMEDIATION; DETECTION METHOD; DNA FINGERPRINTING; ENZYME; ENZYME ACTIVITY; NAPHTHALENE; PAH; PHENANTHRENE; PYRENE; SOIL REMEDIATION;

ARTICLE; BACTERIAL GENE; BACTERIUM CULTURE; BIODEGRADATION; BIOREMEDIATION; CONTROLLED STUDY; DENATURING GRADIENT GEL ELECTROPHORESIS; DNA EXTRACTION; GAS CHROMATOGRAPHY; GENE AMPLIFICATION; GENE INSERTION; GENE LIBRARY; MICROBIAL DEGRADATION; MICROBIAL DIVERSITY; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; POLYMERASE CHAIN REACTION;

BACTERIA; BIODEGRADATION, ENVIRONMENTAL; DIOXYGENASES; DNA PRIMERS; DNA, RIBOSOMAL; KINETICS; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLYCYCLIC HYDROCARBONS, AROMATIC; POLYMERASE CHAIN REACTION; RNA, RIBOSOMAL, 16S;

BACTERIA (MICROORGANISMS);

EID: 33745132697     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.02969-05     Document Type: Article

References (58)

1. Ahn, Y., J. Sanseverino, and G. S. Sayler. 1999. Analyses of polycyclic aromatic hydrocarbon-degrading bacteria isolated from contaminated soils. Biodegradation 10:149-157.
2. Allen, C. C. R., D. R. Boyd, M. J. Larkin, K. A. Reid, N. D. Sharma, and K. Wilson. 1997. Metabolism of naphthalene, 1-naphthol, indene, and indole by Rhodococcus sp. strain NCIMB 12038. Appl. Environ. Microbiol. 63:151-155.
3. Armengaud, J., B. Happe, and K. N. Timmis. 1998. Genetic analysis of dioxin dioxygenase of Sphingomonas sp. strain RW1: catabolic genes dispersed on the genome. J. Bacteriol. 180:3954-3966.
4. Baldwin, B. R., C. H. Nakatsu, and L. Nies. 2003. Detection and enumeration of aromatic oxygenase genes by multiplex and real-time PCR. Appl. Environ. Microbiol. 69:3350-3358.
5. Bodour, A. A., J. M. Wang, M. L. Brusseau, and R. M. Maier. 2003. Temporal change in culturable phenanthrene degraders in response to long-term exposure to phenanthrene in a soil column system. Environ. Microbiol. 5:888-895.
6. Boonchan, S., M. L. Britz, and G. A. Stanley. 1998. Surfactant-enhanced biodegradation of high molecular weight polycyclic aromatic hydrocarbons by Stenotrophomonas maltophilia. Biotechnol. Bioeng. 59:482-494.
7. Bosch, R., E. Garcia-Valdes, and E. R. Moore. 1999. Genetic characterization and evolutionary implications of a chromosomally encoded naphthalene-degradation upper pathway from Pseudomonas stutzeri AN10. Gene 236:149-157.
8. Brezna, B., A. A. Khan, and C. E. Cerniglia. 2003. Molecular characterization of dioxygenases from polycyclic aromatic hydrocarbon-degrading Mycobacterium spp. FEMS Microbiol. Lett. 223:177-183.
9. Cerniglia, C. E. 1992. Biodegradation of polycyclic aromatic hydrocarbons. Biodegradation 3:351-368.
10. Chao, A. 1984. Non-parametric estimation of the number of classes in a population. Scand. J. Stat. 11:265-270.
11. Chao, A., and S. M. Lee. 1992. Estimating the number of classes via sample coverage. J. Am. Stat. Assoc. 87:210-217.
12. Cigolini, J. F., A. K. Goyal, and G. J. Zylstra. 1997. Universal PCR primers for detection, identification, and cloning of genes for dioxygenase enzymes involved in ring oxidation of aromatic compounds. Abstr. 97th Gen. Meet. Am. Soc. Microbiol. 1997, abstr. Q-49, p. 463.
13. Collins, J. F., J. B. Brown, G. V. Alexeeff, and A. G. Salmon. 1998. Potency equivalency factors for some polycyclic aromatic hydrocarbons and polycyclic aromatic hydrocarbon derivatives. Regul. Toxicol. Pharmacol. 28:45-54.
14. Dennis, J. J., and G. J. Zylstra. 2004. Complete sequence and genetic organization of pDTG1, the 83 kilobase naphthalene degradation plasmid from Pseudomonas putida strain NCIB 9816-4. J. Mol. Biol. 341:753-768.
15. Di Gregorio, S., C. Zocca, S. Sidler, A. Toffanin, D. Lizzari, and G. Vallini. 2004. Identification of two new sets of genes for dibenzothiophene transformation in Burkholderia sp. DBT1. Biodegradation 15:111-123.
16. Dibble, A. S., C. Cheng, and C. A. H. Biggar. 1990. Polycyclic aromatic hydrocarbon carcinogens, p. 109-127. In M. W. Pariza, H. U. Aeschbacher, J. S. Fenton, and S. Sato (ed.), Mutagens and carcinogens in the diet. Wiley-Liss, New York, N.Y.
17. Dionisi, H., C. Chewning, K. Morgan, F. Menn, J. Easter, and G. Sayler. 2004. Abundance of dioxygenase genes similar to Ralstonia sp. strain U2 nagAc is correlated with naphthalene concentrations in coal tar-contaminated freshwater sediments. Appl. Environ. Microbiol. 70:3988-3995.
18. Dunbar, J., S. White, and L. Forney. 1997. Genetic diversity through the looking glass: effect of enrichment bias. Appl. Environ. Microbiol. 63:1326-1331.
19. Ferraro, D. J., L. Gakhar, and S. Ramaswamy. 2005. Rieske business: structure-function of Rieske non-heme oxygenases. Biochem. Biophys. Res. Commun. 338:175-190.
20. Ferrero, M., E. Llobet-Brossa, J. Lalucat, E. Garcia-Valdes, R. Rossello-Mora, and R. Bosch. 2002. Coexistence of two distinct copies of naphthalene degradation genes in Pseudomonas strains isolated from the western Mediterranean region. Appl. Environ. Microbiol. 68:957-962.
21. Gibson, D. T., and R. E. Parales. 2000. Aromatic hydrocarbon dioxygenases in environmental biotechnology. Curr. Opin. Biotechnol. 11:236-243.
22. Greene, E., J. Kay, K. Jaber, L. Stehmeier, and G. Voordouw. 2000. Composition of soil microbial communities enriched on a mixture of aromatic hydrocarbons. Appl. Environ. Microbiol. 66:5282-5289.
23. Harder, W., and L. Dijkhuizen. 1982. Strategies of mixed substrate utilization in microorganisms. Philos. Trans. R. Soc. Lond. B Biol. Sci. 297:459-480.
24. Jeon, C. O., W. Park, P. Padmanabhan, C. DeRito, J. R. Snape, and E. L. Madsen. 2003. Discovery of a bacterium, with distinctive dioxygenase, that is responsible for in situ biodegradation in contaminated sediment. Proc. Natl. Acad. Sci. USA 100:13591-13596.
25. Juhasz, A. L., and R. Naidu. 2000. Bioremediation of high molecular weight polycyclic aromatic hydrocarbons: a review of the microbial degradation of benzo[a]pyrene. Int. Biodeterior. Biodegrad. 45:57-88.
26. Kanaly, R. A., R. Bartha, K. Watanabe, and S. Harayama. 2000. Rapid mineralization of benzo[a]pyrene by a microbial consortium growing on diesel fuel. Appl. Environ. Microbiol. 66:4205-4211.
27. Kasuga, K., H. Habe, J. S. Chung, T. Yoshida, H. Nojiri, H. Yamane, and T. Omori. 2001. Isolation and characterization of the genes encoding a novel oxygenase component of angular dioxygenase from the gram-positive dibenzofuran-degrader Terrabacter sp. strain DBF63. Biochem. Biophys. Res. Commun. 283:195-204.
28. Kauppi, B., K. Lee, E. Carredano, R. E. Parales, D. T. Gibson, H. Eklund, and S. Ramaswamy. 1998. Structure of an aromatic-ring-hydroxylating dioxygenase-naphthalene 1,2-dioxygenase. Struct. Fold. Des. 6:571-586.
29. Khan, A. A., R. F. Wang, W. W. Cao, D. R. Doerge, D. Wennerstrom, and C. E. Cerniglia. 2001. Molecular cloning, nucleotide sequence, and expression of genes encoding a polycyclic aromatic ring dioxygenase from Mycobacterium sp. strain PYR-1. Appl. Environ. Microbiol. 67:3577-3585.
30. Kim, D. Y., J. C. Chae, G. J. Zylstra, Y. S. Kim, S. H. Kim, M. H. Nam, Y. M. Kim, and E. B. Kim. 2004. Identification of a novel dioxygenase involved in metabolism of o-xylene, toluene, and ethylbenzene by Rhodococcus sp. strain DK17. Appl. Environ. Microbiol. 70:7086-7092.
31. Krebs, C. J., and J. Brzustowski. The rarefaction calculator. [Online.] http: //www2.biology.ualberta.ca/jbrzusto/rarefact.php.
32. Kumar, S., K. Tamura, and M. Nei. 2004. MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief. Bioinform. 5:150-163.
33. Laurie, A. D., and G. Lloyd-Jones. 1999. The phn genes of Burkholderia sp. strain RP007 constitute a divergent gene cluster for polycyclic aromatic hydrocarbon catabolism. J. Bacteriol. 181:531-540.
34. Laurie, A. D., and G. Lloyd-Jones. 2000. Quantification of phnAc and nahAc in contaminated New Zealand soils by competitive PCR. Appl. Environ. Microbiol. 66:1814-1817.
35. Lee, K. U., B. Kauppi, R. E. Parales, D. T. Gibson, and S. Ramaswamy. 1997. Purification and crystallization of the oxygenase component of naphthalene dioxygenase in native and selenomethionine-derivatized forms. Biochem. Biophys. Res. Commun. 241:553-557.
36. Lloyd-Jones, G., A. D. Laurie, D. W. F. Hunter, and R. Fraser. 1999. Analysis of catabolic genes for naphthalene and phenanthrene degradation in contaminated New Zealand soils. FEMS Microbiol. Ecol. 29:69-79.
37. Meyer, S., R. Moser, A. Neef, U. Stahl, and P. Kampfer. 1999. Differential detection of key enzymes of polyaromatic-hydrocarbon-degrading bacteria using PCR and gene probes. Microbiology 145:1731-1741.
38. Mueller, J. G., R. Devereux, D. L. Santavy, S. E. Lantz, S. G. Willis, and P. H. Pritchard. 1997. Phylogenetic and physiological comparisons of PAH-degrading bacteria from geographically diverse soils. Antonie Leeuwenhoek 71:329-343.
39. Muyzer, G., S. Hottentrager, A. Teske, and C. Wawer. 1996. Denaturing gradient gel electrophoresis of PCR amplified 16S rDNA: a new molecular approach to analyze the genetic diversity of mixed microbial communities. In A. D. L. Akkermans, J. D. Van Elsas, and F. J. de Bruijn (ed.), Molecular microbial ecology manual. Kluwer Academic Publishing, Dordrecht, The Netherlands.
40. Nam, J. W., H. Nojiri, T. Yoshida, H. Habe, H. Yamane, and T. Omori. 2001. New classification system for oxygenase components involved in ring-hydroxylating oxygenations. Biosci. Biotechnol. Biochem. 65:254-263.
41. Nojiri, H., H. Habe, and T. Omori. 2001. Bacterial degradation of aromatic compounds via angular dioxygenation. J. Gen. Appl. Microbiol. 47:279-305.
42. Parales, R. E. 2003. The role of active-site residues in naphthalene dioxygenase. J. Ind. Microbiol. Biotechnol. 30:271-278.
43. Parales, R. E., K. Lee, S. M. Resnick, H. Y. Jiang, D. J. Lessner, and D. T. Gibson. 2000. Substrate specificity of naphthalene dioxygenase: effect of specific amino acids at the active site of the enzyme. J. Bacteriol. 182:1641-1649.
44. Pielou, E. C. 1977. Mathematical ecology, 2nd ed. Wiley, New York, N.Y.
45. Porter, K. G., and Y. S. Feig. 1980. The use of DAPI for identifying and counting aquatic microflora. Limnol. Oceanogr. 25:943-948.
46. Romine, M. F., L. C. Stillwell, K. K. Wong, S. J. Thurston, E. C. Sisk, C. Sensen, T. Gaasterland, J. K. Fredrickson, and J. D. Saffer. 1999. Complete sequence of a 184-kilobase catabolic plasmid from Sphingomonas aromaticivorans F199. J. Bacteriol. 181:1585-1602.
47. Sato, S., N. Ouchiyama, T. Kimura, H. Nojiri, H. Yamane, and T. Omori. 1997. Cloning of genes involved in carbazole degradation of Pseudomonas sp. strain CA10: nucleotide sequences of genes and characterization of meta-cleavage enzymes and hydrolase. J. Bacteriol. 179:4841-4849.
48. Shuttleworth, K. L., and C. E. Cerniglia. 1995. Environmental aspects of PAH biodegradation. Appl. Biochem. Biotechnol. 54:291-302.
49. Simon, M. J., T. D. Osslund, R. Saunders, B. D. Ensley, S. Suggs, A. Harcourt, W. C. Suen, D. L. Cruden, D. T. Gibson, and G. J. Zylstra. 1993. Sequences of genes encoding naphthalene dioxygenase in Pseudomonas putida strains G7 and NCIB 9816-4. Gene 27:31-37.
50. Stach, J. E. M., and R. G. Burns. 2002. Enrichment versus biofilm culture: a functional and phylogenetic comparison of polycyclic aromatic hydrocarbon-degrading microbial communities. Environ. Microbiol. 4:169-182.
51. Stanier, R. Y., N. J. Palleroni, and M. Doudoroff. 1966. The aerobic pseudomonads: a taxonomic study. J. Gen. Appl. Microbiol. 43:159-271.
52. Stapleton, R., and G. Sayler. 1998. Assessment of the microbiological potential for the natural attenuation of petroleum hydrocarbons in a shallow aquifer system. Microb. Ecol. 36:349-361.
53. Stoffels, M., R. Amann, W. Ludwig, D. Hekmat, and K. H. Schleifer. 1998. Bacterial community dynamics during start-up of a trickle-bed bioreactor degrading aromatic compounds. Appl. Environ. Microbiol. 64:930-939.
54. Tuomi, P. M., J. M. Salminen, and K. S. Jorgensen. 2004. The abundance of nahAc genes correlates with the C-14-naphthalene mineralization potential in petroleum hydrocarbon-contaminated oxic soil layers. FEMS Microbiol. Ecol. 51:99-107.
55. Widada, J., H. Nojiri, K. Kasuga, T. Yoshida, H. Habe, and T. Omori. 2002. Molecular detection and diversity of polycyclic aromatic hydrocarbon-degrading bacteria isolated from geographically diverse sites. Appl. Microbiol. Biotechnol. 58:202-209.
56. Wilson, M. S., C. Bakermans, and E. L. Madsen. 1999. In situ, real-time catabolic gene expression: extraction and characterization of naphthalene dioxygenase mRNA transcripts from groundwater. Appl. Environ. Microbiol. 65:80-87.
57. Ye, D. Y., M. A. Siddiqi, A. E. Maccubbin, S. Kumar, and H. C. Sikka. 1996. Degradation of polynuclear aromatic hydrocarbons by Sphingomonas paucimobilis. Environ. Sci. Technol. 30:136-142.
58. Zocca, C., S. Di Gregorio, F. Visentini, and G. Vallini. 2004. Biodiversity amongst cultivable polycyclic aromatic hydrocarbon-transforming bacteria isolated from an abandoned industrial site. FEMS Microbiol. Lett. 238:375-382.