Evolutionary relationship between chlorocatechol catabolic enzymes from Rhodococcus opacus 1CP and their counterparts in proteobacteria: Sequence divergence and functional convergence

Journal of Bacteriology

Volumn 180, Issue 5, 1998, Pages 1082-1094

  Eulberg, Dirk ^a   Kourbatova, Elena M ^b,c   Golovleva, Ludmila A ^b   Schlömann, Michael ^a  

^a UNIVERSITY OF STUTTGART   (Germany)

^b RUSSIAN ACADEMY OF SCIENCES   (Russian Federation)

^c PUSHCHINO STATE UNIVERSITY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL GENE; ENZYME ANALYSIS; EVOLUTION; GENE CLUSTER; HYPOTHESIS; MOLECULAR CLONING; NONHUMAN; OPEN READING FRAME; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RHODOCOCCUS;

ACTINOBACTERIA (CLASS); BACTERIA (MICROORGANISMS); ERYTHROPOLIS; POSIBACTERIA; PROKARYOTA; PROTEOBACTERIA; RHODOCOCCUS OPACUS; UNCULTURED ACTINOMYCETE;

EID: 0031884484     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/jb.180.5.1082-1094.1998     Document Type: Article

References (75)

1. Aldrich, T. L., and A. M. Chakrabarty. 1988. Transcriptional regulation, nucleotide sequence, and localization of the promoter of the catBC operon in Pseudomonas putida. J. Bacteriol. 170:1297-1304.
2. Alting-Mees, M. A., J. A. Sorge, and J. M. Short. 1992. pBluescriptII: multifunctional cloning and mapping vectors. Methods Enzymol. 216:483-495.
3. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
4. Amy, P. S., J. W. Schulke, L. M. Frazier, and R. J. Seidler. 1985. Characterization of aquatic bacteria and cloning of genes specifying partial degradation of 2,4-dichlorophenoxyacetic acid. Appl. Environ. Microhiol. 49: 1237-1245.
5. Bethesda Research Laboratories. 1986. BRL pUC host: E. coli DH5α competent cells. Bethesda Res. Lab. Focus 8(2):9.
6. Chatterjee, D. K., and A. M. Chakrabarty. 1982. Genetic rearrangements in plasmids specifying total degradation of chlorinated benzoic acids. Mol. Gen. Genet. 188:279-285.
7. Chen, C. W., T.-W. Yu, H.-M. Chung, and C.-F. Chou. 1992. Discovery and characterization of a new transposable element, Tn4811, in Streptomyces lividans 66. J. Bacteriol. 174:7762-7769.
8. Coco, W. M., R. K. Rothmel, S. Henikoff, and A. M. Chakrabarty. 1993. Nucleotide sequence and initial functional characterization of the clcR gene encoding a LysR family activator of the clcABD chlorocatechol operon in Pseudomonas putida. J. Bacteriol. 175:417-427.
9. Coucheron, D. H. 1993. A family of IS1031 elements in the genome of Acetobacter xylinum: nucleotide sequences and strain distribution. Mol. Microbiol. 9:211-218.
10. D'Aquila, R. T., L. J. Bechtel, J. A. Videler, J. J. Eron, P. Gorczyca, and J. C. Kaplan. 1991. Maximizing sensitivity and specificity of PCR by preamplification heating. Nucleic Acids Res. 19:3749.
11. Don, R. H., A. J. Weightman, H.-J. Knackmuss, and K. N. Timmis. 1985. Transposon mutagenesis and cloning analysis of the pathways for degradation of 2,4-dichlorophenoxyacetic acid and 3-chlorobenzoate in Alcaligenes eutrophus JMP134(pJP4). J. Bacteriol. 161:85-90.
12. Doolittle, R. F. 1994. Convergent evolution: the need to be explicit. Trends Biochem. Sci. 19:15-18.
13. Dorn, E., and H.-J. Knackmuss. 1978. Chemical structure and biodegradability of halogenated aromatic compounds. Substituent effects on 1,2-dioxygenation of catechol. Biochem. J. 174:85-94.
14. Eck, R., and J. Belter. 1993. Cloning and characterization of a gene coding for the catechol 1,2-dioxygenase of Arthrobacter sp. mA3. Gene 123:87-92.
15. Ehrt, S., F. Schirmer, and W. Hillen. 1995. Genetic organization, nucleotide sequence and regulation of expression of genes encoding phenol hydroxylase and catechol 1,2-dioxygenase in Acinetobacter calcoaceticus NCIB8250. Mol. Microbiol. 18:13-20.
16. Eulberg, D., and M. Schlömann. 1997. Convergent evolution of chlorocatechol catabolism in Rhodococcus and proteobacteria. Biospektrum (special issue), abstr. VU016, p. 35.
17. Eulberg, D., L. A. Golovleva, and M. Schlömann. 1997. Characterization of catechol catabolic genes from Rhodococcus erythropolis 1CP. J. Bacteriol. 179:370-381.
18. Eulberg, D., S. Lakner, L. A. Golovleva, and M. Schlömann. 1998. Characterization of a protocatechuate catabolic gene cluster from Rhodococcus opacus 1CP: evidence for a merged enzyme with 4-carboxymuconolactonedecarboxylating and 3-oxoadipate enol-lactone-hydrolyzing activity. J. Bacteriol. 180:1072-1081.
19. Felsenstein, J. 1993. PHYLIP (Phylogeny Inference Package) version 3.5c. Distributed by the author. Department of Genetics, University of Washington, Seattle, Wash.
20. Frantz, B., and A. M. Chakrabarty. 1987. Organization and nucleotide sequence determination of a gene cluster involved in 3-chlorocatechol degradation. Proc. Natl. Acad. Sci. USA 84:4460-4464.
21. Fulthorpe, R. R., C. McGowan, O. V. Maltseva, W. E. Holben, and J. M. Tiedje. 1995. 2,4-Dichlorophenoxyacetic acid-degrading bacteria contain mosaics of catabolic genes. Appl. Environ. Microbiol. 61:3274-3281.
22. Gerlt, J. A., and P. G. Gassman. 1992. Understanding enzyme-catalyzed proton abstraction from carbon acids: details of stepwise mechanisms for β-elimination reactions. J. Am. Chem. Soc. 114:5928-5934.
23. Ghisalba, O. 1983. Chemical wastes and their biodegradation - an overview. Experientia 39:1247-1257.
24. Gish, W., and D. J. States. 1993. Identification of protein coding regions by database similarity search. Nat. Genet. 3:266-272.
25. Gorlatov, S. N., O. V. Maltseva, V. I. Shevchenko, and L. A. Golovleva. 1989. Degradation of chlorophenols by a culture of Rhodococcus erythropolis. Mikrobiologiya 58:802-806. (Microbiology 58:647-651.)
26. Gorlatov, S. N., O. V. Maltseva, V. I. Shevchenko, and L. A. Golovleva. 1989. Degradation of chlorophenols by a culture of Rhodococcus erythropolis. Mikrobiologiya 58:802-806. (Microbiology 58:647-651.)
27. Häggblom, M. M. 1992. Microbial breakdown of halogenated aromatic pesticides and related compounds. FEMS Mierobiol. Rev. 103:29-72.
28. Hammer, A., T. Hildenbrand, H. Hoier, K.-L. Ngai, M. Schlömann, and J. J. Stezowski. 1993. Crystallization and preliminary X-ray data of chloromuconate cycloisomerase from Alcaligenes eutrophus JMP134 (pJP4). J. Mol. Biol. 232:305-307.
29. Hartnett, C., E. L. Neidle, K.-L. Ngai, and L. N. Ornston. 1990. DNA sequences of genes encoding Acinetobacter calcoaceticus protocatechuate 3,4-dioxygenase: evidence indicating shuffling of genes and of DNA sequences within genes during their evolutionary divergence. J. Bacteriol. 172:956-966.
30. Hartnett, G. B., and L. N. Ornston. 1994. Acquisition of apparent DNA slippage structures during extensive evolutionary divergence of pcaD and catD genes encoding identical catalytic activities in Acinetobacter calcoaceticus. Gene 142:23-29.
31. Helin, S., P. C. Kahn, B. L. Guha, D. G. Mallows, and A. Goldman. 1995. The refined X-ray structure of muconate lactonizing enzyme from Pseudomonas putida PRS2000 at 1.85 Å resolution. J. Mol. Biol. 254:918-941.
32. Higgins, D. G., and P. M. Sharp. 1989. Fast and sensitive multiple sequence alignments on a microcomputer. CABIOS 5:151-153.
33. Hinner, I.-S., M. Lohmann, and M. Schlömann. 1997. Two catechol catabolic genes in Ralstonia eutropha 335. Biospektrum (special issue), abstr. PU074, p. 71.
34. Hoier, H., M. Schlömann, A. Hammer, J. P. Glusker, H. L. Carrell, A. Goldman, J. J. Stezowski, and U. Heinemann. 1994. Crystal structure of chloromuconate cycloisomerase from Alcaligenes eutrophus JMP134 (pJP4) at 3 Å resolution. Acta Crystallogr. D50:75-84.
35. Holben, W. E., B. M. Schroeter, V. G. M. Calabrese, R. H. Olsen, J. K. Kukor, V. O. Biederbeck, A. E. Smith, and J. M. Tiedje. 1992. Gene probe analysis of soil microbial populations selected by amendment with 2,4-dichlorophenoxyacetic acid. Appl. Environ. Microbiol. 58:3941-3948.
36. Houghton, J. E., T, M. Brown, A. J. Appel, E. J. Hughes, and L. N. Ornston. 1995. Discontinuities in the evolution of Pseudomonas putida cat genes. J. Bacteriol. 177:401-412.
37. Ka, J. O., W. E. Holben, and J. M. Tiedje. 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. 60:1106-1115.
38. Kivisaar, M., L. Kasak, and A. Nurk. 1991. Sequence of the plasmid-encoded catechol 1,2-dioxygenase-expressing gene, pheB, of phenol-degrading Pseudomonas sp. strain EST1001. Gene 98:15-20.
39. Kõiv, V., R. Marits, and A. Heinaru. 1996. Sequence analysis of the 2,4-dichlorophcnol hydroxylase gene tfdB and 3,5-dichlorocatechol 1,2-dioxygenase gene tfdC of 2,4-dichlorophenoxyacetic acid degrading plasmid pEST4011. Gene 174:293-297.
40. Kuhm, A. E., M. Schlömann, H.-J. Knackmuss, and D. H. Pieper. 1990. Purification and characterization of dichloromuconate cycloisomerase from Alcaligenes eutrophus JMP 134. Biochem. J. 266:877-883.
41. Leveau, J. H. J., and J. R. van der Meer. 1996. The tfdR gene product can successfully take over the role of the insertion element-inactivated TfdT protein as a transcriptional activator of the tfdCDEF gene cluster, which encodes chlorocatechol degradation in Ralstonia eutropha JMP134(pJP4). J. Bacteriol. 178:6824-6832.
42. Lipscomb, J. D., and A. M. Orville. 1992. Mechanistic aspects of dihydroxybenzoate dioxygenases, p. 243-298. In H. Sigel and A. Sigel (ed.), Metal ions in biological systems, vol. 28. Degradation of environmental pollutants by microorganisms and their metalloenzymes. Marcel Dekker, Inc., New York, N.Y.
43. Mäe, A. A., R. O. Marits, N. R. Ausmees, V. M. Kõiv, and A. L. Heinaru. 1993. Characterization of a new 2,4-dichlorophenoxyacetic acid degrading plasmid pEST4011: physical map and localization of catabolic genes. J. Gen. Microbiol. 139:3165-3170.
44. Maltseva, O. V., I. P. Solyanikova, and L. A. Golovleva. 1994. Chlorocatechol 1,2-dioxygenase from Rhodococcus erythropolis 1CP. Kinetic and immunochemical comparison with analogous enzymes from Gram-negative strains. Eur. J. Biochem. 226:1053-1061.
45. Maltseva, O. V., I. P. Solyanikova, L. A. Golovleva, M. Schlömann, and H.-J. Knackmuss. 1994. Dienelactone hydrolase from Rhodococcus erythropolis 1CP: purification and properties. Arch. Microbiol. 162:368-374.
46. Marchuk, D., M. Drumm, A. Saulino, and F. S. Collins. 1991. Construction of T-vectors, a rapid and general system for direct cloning of unmodified PCR products. Nucleic Acids Res. 19:1154.
47. Matrubutham, U., and A. R. Harker. 1994. Analysis of duplicated gene sequences associated with tfdR and tfdS in Alcaligenes eutrophus JMP134. J. Bacteriol. 176:2348-2353.
48. + aniline-assimilating Rhodococcus erythropolis AN-13. Gene 185:49-54.
49. Nakai, C., H. Uyeyama, H. Kagamiyama, T. Nakazawa, S. Inouye, F. Kishi, A. Nakazawa, and M. Nozaki. 1995. Cloning, DNA sequencing, and amino acid sequencing of catechol 1,2-dioxygenases (pyrocatechase) from Pseudomonas putida mt-2 and Pseudomonas arvilla C-1. Arch. Biochem. Biophys. 321:353-362.
50. Neidle, E. L., C. Hartnett, S. Bonitz, and L. N. Ornston. 1988. DNA sequence of the Acinetobacter calcoaceticus catechol 1,2-dioxygenase I structural gene catA: evidence for evolutionary divergence of intradiol dioxygenases by acquisition of DNA sequence repetitions. J. Bacteriol. 170:4874-4880.
51. Ollis, D. L., E. Cheah, M. Cygler, B. Dijkstra, F. Frolow, S. M. Franken, M. Harel, S. J. Remington, I. Silman, J. Schrag, J. L. Sussman, K. H. G. Verschueren, and A. Goldman. 1992. The α/β hydrolase fold. Protein Eng. 5:197-211.
52. Pearson, W. R., and D. J. Lipman. 1988. Improved tools for biological sequence comparison. Proc. Natl. Acad. Sci. USA 85:2444-2448.
53. Perkins, E. J., M. P. Gordon, O. Caceres, and P. F. Lurquin. 1990. Organization and sequence analysis of the 2,4-dichlorophenol hydroxylase and dichlorocatechol oxidative operons of plasmid pJP4. J. Bacteriol. 172:2351-2359.
54. Pieper, D. H., W. Reineke, K.-H. Engesser, and H.-J. Knackmuss. 1988. Metabolism of 2,4-dichlorophenoxyacetic acid, 4-chloro-2-methylphenoxyacetic acid and 2-methylphenoxyacetic acid by Alcaligenes eutrophus JMP 134. Arch. Microbiol. 150:95-102.
55. Reineke, W. 1994. Degradation of chlorinated aromatic compounds by bacteria: strain development, p. 416-454. In G. R. Chaudhry (ed.), Biological degradation and bioremediation of toxic chemicals. Dioscorides Press, Portland, Oreg.
56. Romero-Arroyo, C. E., M. A. Schell, G. L. Gaines III, and E. L. Neidle. 1995. catM encodes a LysR-type transcriptional activator regulating catechol degradation in Acinetobacter calcoaceticus. J. Bacteriol. 177:5891-5898.
57. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
58. Schell, U. Unpublished results.
59. Schlömann, M. 1994. Evolution of chlorocatechol catabolic pathways. Conclusions to be drawn from comparisons of lactone hydrolases. Biodegradation 5:301-321.
60. Schlömann, M., E. Schmidt, and H.-J. Knackmuss. 1990. Different types of dienelactone hydrolase in 4-fluorobenzoate-utilizing bacteria. J. Bacteriol. 172:5112-5118.
61. Schmidt, E., and H.-J. Knackmuss. 1980. Chemical structure and biodegradability of halogenated aromatic compounds. Conversion of chlorinated muconic acids into maleoylacetic acid. Biochem. J. 192:339-347.
62. Seibert, V., L. A. Golovleva, and M. Schlömann. 1995. Cloning of maleylacetate reductase genes from Alcaligenes eutrophus JMP289 and Rhodococcus erythropolis 1CP. Biospektrum (special issue), abstr. PA013, p. 57.
63. Shanley, M. S., A. Harrison, R. E. Parales, G. Kowalchuk, D. J. Mitchell, and L. N. Ornston. 1994. Unusual G+C content and codon usage in catIJF, a segment of the ben-cat supra-operonic cluster in the Acinetobacter calcoaceticus chromosome. Gene 138:59-65.
64. Solyanikova, I. P., O. V. Maltseva, M. D. Vollmer, L. A. Golovleva, and M. Schlömann. 1995. Characterization of muconate and chloromuconate cycloisomerase from Rhodococcus erythropolis 1CP: indications for functionally convergent evolution among bacterial cycloisomerases. J. Bacteriol. 177: 2821-2826.
65. Stone, K. L., M. B. LoPresti, J. M. Crawford, R. DeAngelis, and K. R. Williams. 1989. Enzymatic digestion of proteins and HPLC peptide isolation, p. 31-47. In P. T. Matsudaira (ed.), A practical guide to protein and peptide purification for microsequencing. Academic Press, Inc., San Diego, Calif.
66. Top, E. M., W. E. Holben, and L. J. Forney. 1995. Characterization of diverse 2,4-dichlorophenoxyacetic acid-degradative plasmids isolated from soil by complementation. Appl. Environ. Microbiol. 61:1691-1698.
67. Tsitko, T. V., G. M. Zaitsev, A. G. Lobanok, and M. S. Salkinoja-Salonen. Tolerance of Rhodococcus opacus strains to aromatic and aliphatic solvents and the role of cellular fatty acids in the adaptation. Submitted for publication.
68. van der Meer, J. R. 1996. Direct submission to the databases.
69. van der Meer, J. R., A. R. W. van Neerven, E. J. de Vries, W. M. de Vos, and A. J. B. Zehnder. 1991. Cloning and characterization of plasmid-encoded genes for the degradation of 1,2-dichloro-, 1.4-dichloro-, and 1,2,4-trichlorobenzene of Pseudomonas sp. strain P51. J. Bacteriol. 173:6-15.
70. van der Meer, J. R., R. I. L. Eggen, A. J. B. Zehnder, and W. M. de Vos. 1991. Sequence analysis of the Pseudomonas sp. strain P51 tcb gene cluster, which encodes metabolism of chlorinated catechols: evidence for specialization of catechol 1,2-dioxygenases for chlorinated substrates. J. Bacteriol. 173:2425-2434.
71. van der Meer, J. R., A. C. J. Frijters, J. H. J. Leveau, R. I. L. Eggen, A. J. B. Zehnder, and W. M. de Vos. 1991. Characterization of the Pseudomonas sp. strain P51 gene tcbR, a LysR-type transcriptional activator of the tcbCDEF chlorocatechol oxidative operon, and analysis of the regulatory region. J. Bacteriol. 173:3700-3708.
72. Varadaraj, K., and D. M. Skinner. 1994. Denaturants or cosolvents improve the specificity of PCR amplification of a G + C-rich DNA using genetically engineered DNA polymerases. Gene 140:1-5.
73. Vollmer, M. D., P. Fischer, H.-J. Knackmuss, and M. Schlömann. 1994. Inability of muconate cycloisomerases to cause dehalogenation during conversion of 2-chloro-cis,cis-muconate. J. Bacteriol. 176:4366-4375.
74. Vollmer, M. D., H. Hoier, U. Schell, J. Gröning, J. Pleiss, A. Goldman, and M. Schlömann. 1995. Differences in the catalytic properties of muconate and chloromuconate cycloisomerases analyzed by site-directed mutagenesis. Biospektrum (special issue), abstr. KV002, p. 24.
75. You, I.-S., and D. Ghosal. 1995. Genetic and molecular analysis of a regulatory region of the herbicide 2,4-dichlorophenoxyacetate catabolic plasmid pJP4. Mol. Microbiol. 16:321-331.