Cis,cis-muconate lactonizing enzyme from Trichosporon cutaneum: evidence for a novel class of cycloisomerases in eucaryotes.

The absolute stereochemical courses of cis,cis-muconate lactonizing enzyme (MLE;EC 5.5.1.1) from Trichosporon cutaneum (TcMLE) and chloromuconate cycloisomerase (MLE II; EC 5.5.1.7) from Pseudomonas sp B13 have been determined from 1H NMR measurements. Both cycloisomerases convert cis,cis-muconate to (4S)-muconolactone by a syn lactonization, the absolute stereochemical outcome of which is identical to that observed with MLE from Pseudomonas putida. The regiochemical courses of cyclization of 3-halo-cis,cis-muconates by TcMLE and MLE II have been characterized and shown to differ in a halogen substituent dependent manner, suggesting at least a different active site architecture of the two MLEs. Moreover, the regiochemical preferences of MLE II and TcMLE parallel results previously observed for the nonenzymatic lactonization of the 3-halomuconates at pH 1-6 and in concentrated HCl, respectively, in which alternate mechanisms of cyclization were proposed [Pieken, W. A., & Kozarich, J. W. (1990) J. Org. Chem. 55, 3029-3035]. Complementary DNA clones encoding TcMLE have been isolated from phenol induced T. cutaneum cDNA using the polymerase chain reaction. The deduced amino acid sequence does not exhibit any similarity to that of MLE from P. putida. It does however, exhibit moderate sequence similarity (21% residue identity, 14 gaps) with 3-carboxy-cis,cis-muconate lactonizing enzyme (CMLE; EC 5.5.1.5) from Neurospora crassa, which catalyzes a regiochemically analogous and stereochemically identical lactonization reaction with 3-carboxymuconate. The limited data available suggest that the fungal CMLE and yeast MLE are representative of a unique class of eucaryotic cycloisomerases which have evolved convergently with the bacterial MLEs.

[1]  W. Thilly,et al.  Fidelity of DNA polymerases in DNA amplification. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[2]  Bruce W. Erickson,et al.  Optimal sequence alignment using affine gap costs , 1986 .

[3]  J. Powlowski,et al.  beta-Ketoadipate pathway in Trichosporon cutaneum modified for methyl-substituted metabolites , 1985, Journal of bacteriology.

[4]  H. Knackmuss,et al.  Chemical structure and biodegradability of halogenated aromatic compounds. Conversion of chlorinated muconic acids into maleoylacetic acid. , 1980, The Biochemical journal.

[5]  J. Powlowski,et al.  Enzymology of the beta-ketoadipate pathway in Trichosporon cutaneum , 1985, Journal of bacteriology.

[6]  J. Lanzillo.  Chemiluminescent nucleic acid detection with digoxigenin-labeled probes: a model system with probes for angiotensin converting enzyme which detect less than one attomole of target DNA. , 1991, Analytical biochemistry.

[7]  R. Kallen,et al.  Enzymes of the beta-ketoadipate pathway in Pseudomonas putida: kinetic and magnetic resonance studies of the cis,cis-muconate cycloisomerase catalyzed reaction. , 1983, Biochemistry.

[8]  B. Frantz,et al.  Cloning and complete nucleotide sequence determination of the catB gene encoding cis,cis-muconate lactonizing enzyme. , 1987, Gene.

[9]  P. Chomczyński,et al.  Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. , 1987, Analytical biochemistry.

[10]  E. Perkins,et al.  Organization and sequence analysis of the 2,4-dichlorophenol hydroxylase and dichlorocatechol oxidative operons of plasmid pJP4 , 1990, Journal of bacteriology.

[11]  F. Sanger,et al.  DNA sequencing with chain-terminating inhibitors. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[12]  H. Neujahr,et al.  cis,cis-Muconate cyclase from Trichosporon cutaneum. , 1980, The Biochemical journal.

[13]  P. Babbitt,et al.  3-Carboxy-cis,cis-muconate lactonizing enzyme from Pseudomonas putida is homologous to the class II fumarase family: a new reaction in the evolution of a mechanistic motif. , 1992, Biochemistry.

[14]  S. Dagley,et al.  Catabolism of L-tyrosine in Trichosporon cutaneum , 1979, Journal of bacteriology.

[15]  P. G. Gassman,et al.  Understanding enzyme-catalyzed proton abstraction from carbon acids: Details of stepwise mechanisms for β-elimination reactions , 1992 .

[16]  B. Orkin,et al.  461. Unsaturated lactones and related substances. Part IV. Lactonic products derived from muconic acid , 1950 .

[17]  J. Kozarich,et al.  Absolute Stereochemical Course of Muconolactone Δ-Isomerase and of 4-carboxymuconolactone Decarboxylase: A H NMR “Ricochet” Analysis , 1987 .

[18]  E. Southern.  Detection of specific sequences among DNA fragments separated by gel electrophoresis. , 1975, Journal of molecular biology.

[19]  J. Kozarich,et al.  Selective synthesis and hydrolysis of dimethyl cis,cis-3-halomuconates , 1989 .

[20]  S. Dagley,et al.  Catabolism of aromatic acids in Trichosporon cutaneum , 1980, Journal of bacteriology.

[21]  E. Neidle,et al.  Characterization of Acinetobacter calcoaceticus catM, a repressor gene homologous in sequence to transcriptional activator genes , 1989, Journal of bacteriology.

[22]  S. Osawa,et al.  Origin and evolution of organisms as deduced from 5S ribosomal RNA sequences. , 1987, Molecular biology and evolution.

[23]  H. N. Fernley,et al.  Bacterial metabolism of 4-chlorophenoxyacetate. , 1971, The Biochemical journal.

[24]  G. Petsko,et al.  Mechanism of the reaction catalyzed by mandelate racemase. 2. Crystal structure of mandelate racemase at 2.5-A resolution: identification of the active site and possible catalytic residues. , 1991, Biochemistry.

[25]  H. Knackmuss,et al.  Chemical structure and biodegradability of halogenated aromatic compounds. Substituent effects on 1,2-dioxygenation of catechol. , 1978, The Biochemical journal.

[26]  J. Kozarich,et al.  Absolute stereochemical course of the 3-carboxymuconate cycloisomerases from Pseudomonas putida and Acinetobacter calcoaceticus: analysis and implications , 1987 .

[27]  Ornston Ln,et al.  Relationships among enzymes of the beta-ketoadipate pathway. I. Properties of cis,cis-muconate-lactonizing enzyme and muconolactone isomerase from Pseudomonas putida. , 1973 .

[28]  T. L. Smith.  Disparate evolution of yeasts and filamentous fungi indicated by phylogenetic analysis of glyceraldehyde-3-phosphate dehydrogenase genes. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[29]  R. B. Cain,et al.  Stereochemistry of enzymic cyclisation of 3-methyl-cis,cis-muconic acid to form 3- and 4-methylmuconolactone , 1989 .

[30]  P. Babbitt,et al.  Mandelate pathway of Pseudomonas putida: sequence relationships involving mandelate racemase, (S)-mandelate dehydrogenase, and benzoylformate decarboxylase and expression of benzoylformate decarboxylase in Escherichia coli. , 1990, Biochemistry.

[31]  W. Pearson.  Rapid and sensitive sequence comparison with FASTP and FASTA. , 1990, Methods in enzymology.

[32]  Gregory A. Petsko,et al.  Mandelate racemase and muconate lactonizing enzyme are mechanistically distinct and structurally homologous , 1990, Nature.

[33]  R. Kallen,et al.  Enzymes of the beta-ketoadipate pathway in Pseudomonas putida: primary and secondary kinetic and equilibrium deuterium isotope effects upon the interconversion of (+)-muconolactone to cis,cis-muconate catalyzed by cis,cis-muconate cycloisomerase. , 1983, Biochemistry.