Characterization of a novel angular dioxygenase from fluorene-degrading Sphingomonas sp. strain LB126

Applied and Environmental Microbiology

Volumn 74, Issue 4, 2008, Pages 1050-1057

  Schuler, Luc ^a   Ní Chadhain, Sinéad M ^b   Jouanneau, Yves ^c   Meyer, Christine ^c   Zylstra, Gerben J ^b   Hols, Pascal ^a   Agathos, Spiros N ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^b RUTGERS UNIVERSITY   (United States)

^c CEA GRENOBLE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC HYDROCARBONS; BACTERIA; COMPLEXATION; DEGRADATION; GENE EXPRESSION; OXIDATION;

DIOXYGENASE COMPLEX; FLUORENE; GRAM-POSITIVE DIBENZOFURAN DEGRADER TERRABACTER;

ENZYMES;

DIBENZOFURAN; DIOXYGENASE; FLUORENE; FLUORENE DERIVATIVE; FLUORENONE DERIVATIVE; PHENANTHRENE; POLYCHLORINATED DIBENZODIOXIN; POLYCYCLIC AROMATIC HYDROCARBON;

BACTERIUM; ENZYME ACTIVITY; GENE; PAH; PHENANTHRENE;

ALPHA CHAIN; AMINO ACID SEQUENCE; ARTICLE; BACTERIAL STRAIN; BETA CHAIN; ESCHERICHIA COLI; GENE FUNCTION; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATION; QUANTITATIVE ANALYSIS; SPHINGOMONAS; TERRABACTER;

BASE SEQUENCE; BLOTTING, SOUTHERN; DIOXYGENASES; DNA PRIMERS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FLUORENES; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; MOLECULAR SEQUENCE DATA; MOLECULAR STRUCTURE; POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY; SPHINGOMONAS;

ESCHERICHIA COLI; POSIBACTERIA; SPHINGOMONAS SP.; TERRABACTER SP.;

EID: 39649117129     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.01627-07     Document Type: Article

References (49)

1. Altschul, S. F., T. L. Madden, A. A. Schaffer, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
2. Ashikawa, Y., Z. Fujimoto, H. Noguchi, H. Habe, T. Omori, H. Yamane, and H. Nojiri. 2006. Electron transfer complex formation between oxygenase and ferredoxin components in Rieske nonheme iron oxygenase system. Structure 14:1779-1789.
3. Bastiaens, L., D. Springael, P. Wattiau, H. Harms, R. deWachter, H. Verachtert, and L. Diels. 2000. Isolation of adherent polycyclic aromatic hydrocarbon (PAH)-degrading bacteria using PAH-sorbing carriers. Appl. Environ. Microbiol. 66:1834-1843.
4. Bunz, P. V., and A. M. Cook. 1993. Dibenzofuran 4,4a-dioxygenase from Sphingomonas sp. strain RW1: angular dioxygenation by a three-component enzyme system. J. Bacteriol. 175:6467-6475.
5. Casellas, M., M. Grifoll, J. M. Bayona, and A. M. Solanas. 1997. New metabolites in the degradation of fluorene by Arthrobacter sp. strain F101. Appl. Environ. Microbiol. 63:819-826.
6. Cerniglia, C. E. 1992. Biodegradation of polycyclic aromatic hydrocarbons. Biodegradation 3:351-368.
7. Demaneche, S., C. Meyer, J. Micoud, M. Louwagie, J. C. Willison, and Y. Jouanneau. 2004. Identification and functional analysis of two aromatic-ring-hydroxylating dioxygenases from a Sphingomonas strain that degrades various polycyclic aromatic hydrocarbons. Appl. Environ. Microbiol. 70:6714-6725.
8. Fortnagel, P., H. Harms, R. M. Wittich, W. Francke, S. Krohn, and H. Meyer. 1989. Cleavage of dibenzofuran and dibenzodioxin ring systems by a Pseudomonas bacterium. Naturwissenschaften 76:222-223.
9. Grifoll, M., M. Casellas, J. M. Bayona, and A. M. Solanas. 1992. Isolation and characterization of a fluorene-degrading bacterium: identification of ring oxidation and ring fission products. Appl. Environ. Microbiol. 58:2910-2917.
10. Grifoll, M., S. Selifonov, and P. Chapman. 1995. Transformation of substituted fluorenes and fluorene analogs by Pseudomonas sp. strain F274. Appl. Environ. Microbiol. 61:3490-3493.
11. Grifoll, M., S. A. Selifonov, and P. J. Chapman. 1994. Evidence for a novel pathway in the degradation of fluorene by Pseudomonas sp. strain F274. Appl. Environ. Microbiol. 60:2438-2449.
12. Grifoll, M., S. A Selifonov, C. V. Gatlin, and P. J. Chapman. 1995. Actions of a versatile fluorene-degrading bacterial isolate on polycyclic aromatic compounds. Appl. Environ. Microbiol. 61:3711-3723.
13. Habe, H., J.-S. Chung, A. Ishida, K. Kasuga, K. Ide, T. Takemura, H. Nojiri, H. Yamane, and T. Omori. 2005. The fluorene catabolic linear plasmid in Terrabacter sp. strain DBF63 carries the beta-ketoadipate pathway genes, pcaRHGBDCFIJ, also found in proteobacteria. Microbiology 151:3713-3722.
14. Habe, H., J. S. Chung, H. Kato, Y. Ayabe, K. Kasuga, T. Yoshida, H. Nojiri, H. Yamane, and T. Omori. 2004. Characterization of the upper pathway genes for fluorene metabolism in Terrabacter sp. strain DBF63. J. Bacteriol. 186:5938-5944.
15. Iida, T., Y. Mukouzaka, K. Nakamura, and T. Kudo. 2002. Plasmid-borne genes code for an angular dioxygenase involved in dibenzofuran degradation by Terrabacter sp. strain YK3. Appl. Environ. Microbiol. 68:3716-3723.
16. Iida, T., K. Nakamura, A. Izumi, Y. Mukouzaka, and T. Kudo. 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.
17. Johnsen, A. R., L. Y. Wick, and H. Harms. 2005. Principles of microbial PAH-degradation in soil. Environ. Pollut. 133:71-84.
18. Jouanneau, Y., C. Meyer, J. Jakoncic, V. Stojanoff, and J. Gaillard. 2006. Characterization of a naphthalene dioxygenase endowed with an exceptionally broad substrate specificity toward polycyclic aromatic hydrocarbons. Biochemistry 45:12380-12391.
19. Kahng, H. Y., K. Nam, J. J. Kukor, B. J. Yoon, D. H. Lee, D. C. Oh, S. K. Kam, and K. H. Oh. 2002. PAH utilization by Pseudomonas rhodesiae KK1 isolated from a former manufactured-gas plant site. Appl. Microbiol. Biotechnol. 60:475-480.
20. 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.
21. Kasuga, K., H. Nojiri, H. Yamane, and T. Omori, 1997. Genes of enzymes involved in the biodegradation of carbazole, dibenzofuran, fluorene, and dibenzo-p-dioxin by bacteria. Water Sci. Technol. 36:9-16.
22. Krivobok, S., S. Kuony, C. Meyer, M. Louwagie, J. C. Willison, and Y. Jouanneau. 2003. Identification of pyrene-induced proteins in Mycobacterium sp. strain 6PY1: evidence for two ring-hydroxylating dioxygenases. J. Bacteriol. 185:3828-3841.
23. Kumar, S., K. Tamura, and M. Nei. 2004. MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief. Bioinform. 5:150-163.
24. Larkin, M. J., C. C. Allen, L. A. Kulakov, and D. A. Lipscomb. 1999. Purification and characterization of a novel naphthalene dioxygenase from Rhodococcus sp. strain NCIMB12038. J. Bacteriol. 181:6200-6204.
25. Marchesi, J. R., T. Sato, A. J. Weightman, T. A. Martin, J. C. Fry, S. J. Hiom, D. Dymock, and W. G. Wade. 1998. Design and evaluation of useful bacterium-specific PCR primers that amplify genes coding for bacterial 16S rRNA. Appl. Environ. Microbiol. 64:795-799.
26. Masai, E., S. Shinohara, H. Hara, S. Nishikawa, Y. Katayama, and M. Fukuda. 1999. Genetic and biochemical characterization of a 2-pyrone-4,6-dicarboxylic acid hydrolase involved in the protocatechuate 4,5-cleavage pathway of Sphingomonas paucimobilis SYK-6. J. Bacteriol. 181:55-62.
27. Mergeay, M., D. Nies, H. G. Schlegel, J. Gerits, P. Charles, and F. Van Gijsegem. 1985. Alcaligenes eutrophus CH34 is a facultative chemolithotroph with plasmid-bound resistance to heavy metals. J. Bacteriol. 162:328-334.
28. Monna, L., T. Omori, and T. Kodama. 1993. Microbial degradation of dibenzofuran, fluorene, and dibenzo-p-dioxin by Staphylococcus auriculans DBF63. Appl. Environ. Microbiol. 59:285-289.
29. Moser, R., and U. Stahl. 2001. Insights into the genetic diversity of initial dioxygenases from PAH-degrading bacteria. Appl. Microbiol. Biotechnol. 55:609-618.
30. Muyzer, G., E. C. de Waal, and A. G. Uitterlinden. 1993. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl. Environ. Microbiol. 59:695-700.
31. Nojiri, H., J. Nam, M. Kosaka, K. Morii, T. Takemura, K. Furihata, H. Yamane, and T. Omori. 1999. Diverse oxygenations catalyzed by carbazole 1,9a-dioxygenase from Pseudomonas sp. strain CA10. J. Bacteriol. 181:3105-3113.
32. Pinyakong, O., H. Habe, A. Kouzuma, H. Nojiri, H. Yamane, and T. Omori. 2004. Isolation and characterization of genes encoding polycyclic aromatic hydrocarbon dioxygenase from acenaphthene and acenaphthylene degrading Sphingomonas sp. strain A4. FEMS Microbiol. Lett. 238:297-305.
33. Pinyakong, O., H. Habe, and T. Omori. 2003. The unique aromatic catabolic genes in sphingomonads degrading polycyclic aromatic hydrocarbons (PAHs). J. Gen. Appl. Microbiol. 49:1-19.
34. Pinyakong, O., H. Habe, N. Supaka, P. Pinpanichkarn, K. Juntongjin, T. Yoshida, K. Furihata, H. Nojiri, H. Yamane, and T. Omori. 2000. Identification of novel metabolites in the degradation of phenanthrene by Sphingomonas sp. strain P2. FEMS Microbiol. Lett. 191:115-121.
35. Resnick, S. M., D. S. Torok, and D. T. Gibson. 1993. Oxidation of carbazole to 3-hydroxycarbazole by naphthalene 1,2-dioxygenase and biphenyl 2,3-dioxygenase. FEMS Microbiol. Lett. 113:297-302.
36. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1990. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
37. Sato, S. I., J. W. Nam, K. Kasuga, H. Nojiri, H. Yamane, and T. Omori. 1997. Identification and characterization of genes encoding carbazole 1,9a-dioxygenase in Pseudomonas sp. strain CA10. J. Bacteriol. 179:4850-4858.
38. Selifonov, S. A., M. Grifoll, J. E. Gurst, and P. J. Chapman. 1993. Isolation and characterization of (+)-1,1a-dihydroxy-1-hydrofluoren-9-one formed by angular dioxygenation in the bacterial catabolism of fluorene. Biochem. Biophys. Res. Commun. 193:67-76.
39. Shepherd, J. M., and G. Lloyd-Jones. 1998. Novel carbazole degradation genes of Sphingomonas CB3: sequence analysis, transcription, and molecular ecology. Biochem. Biophys. Res. Commun. 247:129-135.
40. Shintani, M., M. Urata, K. Inoue, K. Eto, H. Habe, T. Omori, H. Yamane, and H. Nojiri. 2007. The Sphingomonas plasmid pCAR3 is involved in complete mineralization of carbazole. J. Bacteriol. 189:2007-2020.
41. Story, S. P., E. L. Kline, T. A. Hughes, M. B. Riley, and S. S. Hayasaka. 2004. Degradation of aromatic hydrocarbons by Sphingomonas paucimobilis strain EPA505. Arch. Environ. Contam. Toxicol. 47:168-176.
42. Story, S. P., S. H. Parker, S. S. Hayasaka, M. B. Riley, and E. L. Kline. 2001. Convergent and divergent points in catabolic pathways involved in utilization of fluoranthene, naphthalene, anthracene, and phenanthrene by Sphingomonas paucimobilis var. EPA505. J. Ind. Microbiol. Biotechnol. 26:369-382.
43. Takagi, T., H. Nojiri, T. Yoshida, H. Habe, and T. Omori. 2002. Detailed comparison between the substrate specificities of two angular dioxygenases, dibenzofuran 4,4a-dioxygenase from Terrabacter sp. and carbazole 1,9a-dioxygenase from Pseudomonas resinovorans. Biotechnol. Lett. 24:2099-2106.
44. Trenz, S. P., K. H. Engesser, P. Fischer, and H. J. Knackmuss. 1994. Degradation of fluorene by Brevibacterium sp. strain DPO 1361: a novel C-C bond cleavage mechanism via 1,10-dihydro-1,10-dihydroxyfluoren-9-one. J. Bacteriol. 176:789-795.
45. van Afferden, M., S. Schacht, J. Klein, and H. G. Trüper. 1990. Degradation of dibenzothiophene by Brevibacterium sp. DO. Arch. Microbiol. 153:324-328.
46. van Herwijnen, R., P. Wattiau, L. Bastiaens, L. Daal, L. Jonker, D. Springael, H. A. Govers, and J. R. Parsons. 2003. Elucidation of the metabolic pathway of fluorene and cometabolic pathways of phenanthrene, fluoranthene, anthracene and dibenzothiophene by Sphingomonas sp. LB126. Res. Microbiol. 154:199-206.
47. Wattiau, P., L. Bastiaens, R. van Herwijnen, L. Daal, J. R. Parsons, M. E. Renard, D. Springael, and G. R. Cornelis. 2001. Fluorene degradation by Sphingomonas sp. LB126 proceeds through protocatechuic acid: a genetic analysis. Res. Microbiol. 152:861-872.
48. Willison, J. C. 2004. Isolation and characterization of a novel sphingomonad capable of growth with chrysene as sole carbon and energy source. FEMS Microbiol. Lett. 241:143-150.
49. Zylstra, G. J., and E. Kim. 1997. Aromatic hydrocarbon degradation by Sphingomonas yanoikuyae B1. J. Ind. Microbiol. Biotechnol. 19:408-414.