, Volume 5, Issue 3–4, pp 259–276 | Cite as

On the origins and functions of the enzymes of the 4-chlorobenzoate to 4-hydroxybenzoate converting pathway

  • Debra Dunaway-Mariano
  • Patricia C. Babbitt


This review examines the enzymes of 4-chlorobenzoate to 4-hydroxybenzoate converting pathway found in certain soil bacteria. This pathway consists of three enzymes: 4-chlorobenzoate: Coenzyme A ligase, 4-chlorobenzoyl-Coenzyme A dehalogenase and 4-hydroxybenzoyl-Coenzyme A thioesterase. Recent progress made in the cloning and expression of the pathway genes from assorted bacterial strains is described. Gene order and sequence found among these strains are compared to reveal independent enzyme recruitment strategies. Sequence alignments made between thePseudomonas sp. strain CBS3 4-chlorobenzoate pathway enzymes and structurally related proteins contained within the protein sequence data banks suggest possible origins in preexisting β-oxidation pathways. The purification and characterization of the physical and kinetic properties of the pathway enzymes are described. Where possible a comparison of these properties between like enzymes from different bacterial sources are made.

Key words

4-chlorobenzoate 4-hydroxybenzoate dehalogenase 4-chlorobenzoyl-CoA dehalogenase 4-chlorobenzoate CoA ligase 4-hydroxyl benzoyl-CoA thioesterase halogenated aromatic degradation nucleophilic aromatic substitution 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Abe T, Fujino T, Fukuyama R, Minoshima S, Shimizu N, Toh N, Hiroyuki S & Yamamoto T (1992) Human long-chain acyl-CoA synthetase: Structure and chromosomal location. J. Biochem. 111: 123–128Google Scholar
  2. Abramowicz DA (1990). Crit. Rev. Biotechnol. 10: 241-Google Scholar
  3. Adriaens P, Kohler H-PE, Kohler-Staub D & Focht DD (1989) Bacterial dehalogenation of chlorobenzoates and coculture biodegradation of 4, 4′-dichlorobiphenyl. Appl. Environ. Microbiol. 55: 887–892Google Scholar
  4. Altenschmidt U & Fuchs G (1992) Novel aerobic 2-aminobenzoate metabolism. Eur. J. Biochem. 205: 721–727Google Scholar
  5. Babbitt PC, Kenyon GL, Martin BM, Charest H, Sylvestre M, Scholten JD, Chang K-H, Liang PH & Dunaway-Mariano D (1992) Ancestry of the 4-chlorobenzoate dehalogenase: analysis of amino acid sequence identities among families of acyl: adenyl ligases, enoyl-CoA hydratases/isomerases and acyl-CoA thioesterases. Biochemistry 31: 5594–5604Google Scholar
  6. Becker-André M, Schulze-Lefert P & Hahlbrock K (1991) Structural comparison, modes of expression, and putativecis-acting elements of the two 4-coumarate: CoA ligase genes in potato. J. Biol. Chem. 266: 8551–8559Google Scholar
  7. Beckman DL & Kranz RG (1991) A bacterial homology to the mitochondrial enoyl-CoA hydratase. Gene 107: 171–172Google Scholar
  8. Birch PR, Sims PF & Broda P (1992) Nucleotide sequences of a gene fromPhanerochaete chrysosporium that shows homology to the xxi gene ofAspergillus nidulans. DNA Sequence 2: 319–323Google Scholar
  9. Black PN, DiRusso CC, Metzger AK & Heimert TL (1992) Cloning, sequencing, and expression for thefadD gene ofEscherichia coli encoding acyl CoA synthetase. J. Biol. 267: 25513–25520Google Scholar
  10. Chang K-H (1994) Purification of a novel 4-chlorobenzoate dehalogenase system and characterization of the 4-chlorobenzoate: CoA ligase. (1994) Ph.D. Thesis, University of MarylandGoogle Scholar
  11. Chang K-H, Liang P-H, Beck W, Scholten JD & Dunaway-Mariano D (1992) Isolation and characterization of the three polypeptide components of 4-chlorobenzoate dehalogenase fromPseudomonas sp. strain CBS-3. Biochemistry 31: 5605–5610Google Scholar
  12. Commandeur LCM & Parsons JR (1990) Degradation of halogenated aromatics. Biodegradation 1: 207-Google Scholar
  13. Connerton IF, Fincham JRS, Sandeman RA & Hynes MJ (1990) Comparison and cross-species expression of the acetyl-CoA synthetase genes of the Ascomycete fungi,Aspergillus nidulans andNeurospora crassa. Mol. Microbiol. 4: 451–460Google Scholar
  14. Copley SD & Crooks GP (1992) Enzymic dehalogenation of 4-chlorobenzoyl Coenzyme A inAcinetobacter sp. strain 4-CB1. Appl. Environ. Microbiol. 58: 1385–1387Google Scholar
  15. Cork DJ & Krueger JP (1991) Microbial transformations of herbicides and pesticides. Adv. App. Microbiol. 36: 1–67Google Scholar
  16. Coque JJ, Martin JF, Calzada JG & Liras P (1991) The cephamycin biosynthetic genes pcbAB, encoding a large multidomain peptide synthetase and pcbC ofNocardia lactamdurans are clustered together in an organization different from the same genes inAcremoium chrysogenum andPenicillin chrysogenum. Mol. Microbiol. 5: 1125–1133Google Scholar
  17. Cosmina P, Rodriguez F, de Ferra F, Grandi G, Perego M, Venema G & van Sinderen D (1993) Sequence and analysis of the genetic locus responsible for surfactin synthesis inBacillus subtilis. Mol. Microbiol. 8: 821–831Google Scholar
  18. Crooks GP & Copley SD (1993) A surprising effect of leaving group on the nucleophilic aromatic substitution reaction catalyzed by 4-chlorobenzoyl-CoA dehalogenase. J. Amer. Chem. Soc. 115: 6422–6423Google Scholar
  19. De Virgilio C, Burckert N, Barth G, Neuhaus JM, Boller & Wiemken A (1992) Cloning and disruption of a gene required for growth on acetate but not on ethanol: the acetyl-CoA synthetase gene ofSaccharomyces cerevisae. Yeast 8: 1043–1051Google Scholar
  20. DeWet JR, Wood KV, DeLuca M, Helinski DR & Subramani S (1987) Firefly luciferase gene: structure and expression in mammalian cells. Mol. Cell Biol. 7: 725–737Google Scholar
  21. Diez B, Gutierrez S, Barredo JL, van Solingen P, van der Voort LH & Martin JF (1990) The cluster of penicillin biosynthetic genes: Identification and characterization of the pcbAB gene encoding the alpha aminoadipyl-cysteinyl-valine synthetase and linkage to the pcbC and penDE genes. J. Biol. Chem. 265: 16358–16365Google Scholar
  22. Dirusso CC (1990) Primary sequence of theEscherichia coli fadBA operon, encoding the fatty acid-oxidizing multienzyme complex, indicates a high degree of homology to eucaryotic enzymes. J. Bacteriol. 172: 6459–6468Google Scholar
  23. Driscoll JR & Taber HW (1992) Sequence organization and regulation of theBacillus subtilis menBE operon. J. Bacteriol. 174: 5063–5071Google Scholar
  24. Duronio RJ, Knoll LJ & Gordon JI (1992) Isolation of aSaccharomyces cerevisiae long chain fatty acyl: CoA synthetase gene (FAA1) and assessment of its role in protein N-myristoylation. J. Cell Biol. 117: 515–529Google Scholar
  25. Eggen RI, Geerling ACM, Boshoven ABP & de Vos WM (1991) Cloning, sequence analysis, and functional expression of the acetyl CoA synthetase gene fromMethanothrix soehngenii in Escherichia coli. J. Bacteriol. 173: 6383–6389Google Scholar
  26. Farrell DH, Mikesell P, Actis LA & Crosa JH (1990) A regulatory gene, angR, of the iron uptake system ofVibrio anguillarum: similarity with phage P22cro and regulation by iron. Gene 86: 45–51Google Scholar
  27. Fujino T & Yamamoto T (1992) Cloning and functional expression of a novel long-chain acyl-CoA synthetase expressed in brain. J. Biochem. 111: 197–203Google Scholar
  28. Fuma S, Fujishima Y, Corbell N, D'Souza C, Nakano MM, Zuber P & Yamane K (1993) Nucleotide sequence of 5′ portion of xi that contains the region required for competence establishment inBacillus subtilus. Nucleic Acids Research 21: 93–97Google Scholar
  29. Furukawa K & Chakrabarty AM (1982) Involvement of plasmids in total degradations of chlorinated biphenyls. Appl. Environ. Microbiol. 44: 619–626Google Scholar
  30. Garre V, Murrillo FJ & Torres-Martinez S (1992) unpublished submission to GenbankGoogle Scholar
  31. Groenewegen PEJ, van den Tweel WJJ & de Bont JAM (1992) Anaerobic bioformation of 4-hydroxybenzoate from 4-chlorobenzoate by thecoryneform bacterium NJB-1. Appl. Microbiol. Biotechnol. 36: 541–547Google Scholar
  32. Grundy FJ, Waters DA, Takova TY & Henkin TM (1993) Identification of genes involved in utilization of acetate and acetoin inBacillus subtilus. Unpublished submission to GenBankGoogle Scholar
  33. Gutierrez S, Diez B, Montenegro E & Martin JF (1991) Characterization of theCephalosporiumacrenonium pcbAB gene encoding alpha-aminoadipyl-cysteinyl-valine synthetase, a large multidomain peptide synthetase: linkage to the pcbC gene as a cluster of early cephalosporin biosynthetic genes and evidence of multiple functional domains. J. Bacteriol. 173: 2354–2365Google Scholar
  34. Haese A, Schubert M, Hermann M & Zocher R (1993) Molecular characterization of the enniatin synthetase gene encoding a multifunctional enzyme catalyzing N-methyldepsipeptide formation inFusarium scirpi. Mol. Microbiol. 7: 905–914Google Scholar
  35. Haggblom MM (1992) Microbial breakdown halogenated aromatic pesticides and related compounds. FEMS Microbiol. Reviews 103: 29–72Google Scholar
  36. Heaton MP & Neuhaus FC (1992) Biosynthesis of D-alanyl-lipoteichoic acid: cloning, nucleotide sequence, and expression of theLactobacillus casei gene for the D-alanine-activating enzyme. J. Bacteriol. 17: 4707–4717Google Scholar
  37. Higson FK (1992) Microbial degradation of biphenyl and its derivatives. Adv. App. Microbiol. 37: 135–165Google Scholar
  38. Hooper SW, Dockendorf JC & Sayler GS (1989) Characteristics and restriction analysis of the 4-chlorobiphenyl catabolic plasmid pSS50. Appl. Environ. Microbiol. 55: 1286–1288Google Scholar
  39. Hori K, Yamamoto Y, Minetoki T, Kurotsu T, Kanda M, Miura S, Okamura K, Furuyama J & Saito Y (1989) Molecular cloning and nucleotide sequence of the gramicidin S synthetase 1 gene. J. Biochem. 106: 639–645Google Scholar
  40. Hori K, Yamamoto Y, Tokita K, Saito F, Kurotsu T, Kanda M, Okamura K, Furuyama J & Saito Y (1991) The nucleotide sequence for a proline-activating domain of gramicidin S synthetase gene from Bacillus brevis. J. Biochem. 110: 111–119Google Scholar
  41. Jackowski S, Jackson PD & Rock CO (1993) Sequence and expression of the 2-acylglycerophosphoelanolamine acyltransferase/acyl-acyl carrier protein synthetase (aas) gene and its role in lysophospholipid acylation inEscherichia coli. Unpubished submission to GenbankGoogle Scholar
  42. Klages U, Krauss S & Lingens F (1983) 2-Haloalkonoic acid dehalogenase from 4-chlorobenzoate degradingPseudomonas sp. CBS-3. Hoppe-Seyler Z. Physiol. Chem. 364: 529–535Google Scholar
  43. Klages U & Lingens F (1980) Degradation of 4-chlorobenzoic acid by aPseudomonas sp. Zentralbl. Bakteriol. Parasitenkd. Infektionskr. Hyg. Abt. 1 Orig. C 1: 215–223Google Scholar
  44. —— (1979) Degradation of 4-chlorobenzoic acid by aNorcardia species. FEMS Microbiol. Lett. 6: 201–203Google Scholar
  45. Klages U, Markus A & Lingens F (1981) Degradation of 4-chlorophenylacetic acid by aPseudomonas species. J. Bacteriol. 146: 64–68Google Scholar
  46. Kraetzchumar J, Krause M & Marahiel MA (1989) Gramicidin S biosynthesis operon containing the structural genes grsA and graB has an open reading frame encoding a protein homologous to fatty acid thioesterases. J. Bacteriol. 171: 5422–5429Google Scholar
  47. Layton AC, Sanseverino J, Wallace W, Corcoran C & Sayler GS (1992) Evidence for 4-chlorobenzoic acid dehalogenation mediated by plasmids related to pSS50. Appl. Environ. Microbiol. 58: 399–402Google Scholar
  48. Liang P-H, Yang G & Dunaway-Mariano D (1993) Specificity of 4-chlorobenzoate-Coenzyme A dehalogenase catalyzed dehalogenation of halogenated aromatics. Biochemistry 32: in pressGoogle Scholar
  49. Liu J, Duncan K & Walsh CT (1989) Nucleotide sequence of a cluster ofEscherichia coli enterobactin biosynthesis genes: identification ofentA and purification of its product 2, 3-dihydro-2, 3-dihydroxybenzoate dehydrogenase. J. Bacteriol. 171: 791–798Google Scholar
  50. Löffler F, Müller R & Lingens F (1992) Purification and properties of 4-halobenzoate-Coenzyme A Ligase fromPseudomonas sp. CBS3. Biol. Chem. Hoppe-Seyler 373: 1001–1007Google Scholar
  51. Lozoya E, Hoffmann H, Douglas C, Schulz W, Scheel D & Hahlbrock K (1988) Primary structures and catalytic properties of isoenzymes encoded by the two 4-coumarate: CoA ligase genes in parsley. Eur. J. Biochem. 176: 661–667Google Scholar
  52. MacCabe AP, van Liempt H, Palissa H, Unkles SE, Riach MDR, Pfeifer E, von Döhren H & Kinghorn JR (1991) Delta (L-alphaminoadipyl)-L-cysteine-D-valine synthetase fromAspergillus nidulans. J. Biol. Chem. 266: 12646–12654Google Scholar
  53. Mallonee DH, White WB & Hylemon PB (1990) Cloning and sequencing of a bile acid-inducible operon fromEubacterium sp. strain VPI 12708. J. Bacteriol. 172: 7011–7019Google Scholar
  54. Manning PA (1991) Unpublished submission to GenbankGoogle Scholar
  55. Marks TS, Smith ARW & Quirk AV (1984) Degradation of 4-chlorobenzoic acid byArthrobacter sp. Appl. Environ. Microbiol. 48: 1020–1025Google Scholar
  56. Markus A, Klages U, Krauss S & Lingens F (1984) Oxidation and dehalogenation of 4-chlorophenylacetate by two-component enzyme systems fromPseudomonas sp. strain CBS-3. J. Bacteriol. 160: 618–621Google Scholar
  57. Masuda T, Tatsumi H & Nakano E (1989) Cloning and sequence analysis of cDNA for luciferase of a Japanese firefly,Luciola cruciata. Gene 77: 265–270Google Scholar
  58. Minami-Ishii N, Taketani S, Osumi T & Hashimoto T (1989) Molecular cloning and sequence analysis of the cDNA for rat mitochondrial enoyl-CoA hydratase. Eur. J. Biochem. 185: 73–78Google Scholar
  59. Morris ME & Jinks-Robertson S (1991) Nucleotide sequence of the LYS2 gene ofSaccharomyces cerevisiae: homology toBacillus brevis tyrocidine synthetase I. Gene 98: 141–145Google Scholar
  60. Müller R, Thiele J, Klages U & Lingens F (1984) Incorporation of [18O] water into 4-hydroxybenzoic acid in the reaction of 4-chlorobenzoate dehalogenase fromPseudomonas sp. CBS3. Biochem. Biophys. Res. Commun. 124: 178–182Google Scholar
  61. Müller R, Oltmanns RH & Lingens F (1988) Enzymatic dehalogenation of 4-chlorobenzoate by extracts fromArthrobacter sp. Su DSM 20407. Biol. Chem. Hoppe-Seyler 369: 567–571Google Scholar
  62. Osumi T, Ishii N, Hijakata M, Kamijos K, Ozasa H, Furuta S, Miyazawa S, Kondo K, Inoue K, Kagamiyama H & Hashimoto T (1985) Molecular cloning and nucleotide sequence of the cDNA for rat peroxisomal enoyl-CoA: hydratase-3-hydroxyacyl-CoA dehydrogenase bifunctional enzyme. J. Biol. Chem. 260: 8905–8910Google Scholar
  63. Palossari PM, Vihinen M, Mäntsälia PI, Alexson SEH, Pihlajanismi T & Hiltunen JK (1991) Amino acid sequence similarities of the mitochondrial short chain δ3, δ2-enoyl-CoA isomerase and peroxisomal multifunctional δ3, δ2-enoyl-CoA isomerase, 2-enoyl-CoA hydratase, 3-hydroxyacyl-CoA dehydrogenase enzyme in rat liver. J. Biol. Chem. 266: 10750–10753Google Scholar
  64. Pettigrew CA, Breen A, Corcoran C & Sayler GS (1990) Chlorinated biphenyl mineralization by individual populations and consortia of fresh water bacteria. Appl. Environ. Microbiol. 56: 2036–3045Google Scholar
  65. Priefert H & Steinbüchel A (1992) Identification and molecular characterization of the aceryl-CoA synthetase gene (acoE) ofAlcaligenes eutrophus. J. Bacteriol. 174: 6590–6599Google Scholar
  66. Ruisinger S, Klager L & Lingens F (1976) Abbau der 4-chlorobenzoesäune durch eineArthrobacter-species. Arch. Microbiol. 110: 253–256Google Scholar
  67. Rusnak F, Sakaitani M, Drueckhammer D, Reichert J & Walsh CT (1991) Biosynthesis of theEscherichia coli siderophore enterobactin: sequence of theentF gene, expression and purification of entF, and analysis of covalent phosphophantetheine. Biochemistry 30: 2916–2927Google Scholar
  68. Sato S, Hayashi M, Imamura S, Ozeki Y & Kawaguchi A (1992) Primary structures of the genes,faoA andfaoB, fromPseudomonas fragiB-0771 which encode the two subunits of the HDT multienzyme complex involved in fatty acid β-oxidation. J. Biochem. 111: 8–15Google Scholar
  69. Savard P, Charest H, Sylvestre M, Shareck F, Scholten JD & Dunaway-Mariano D (1992) Expression of the 4-chlorobenzoate dehalogenase genes ofPseudomonas sp. CBS3 inEscherichia coli and identification of the gene translation products. Can. J. Microbiol. 38: 1074–1083Google Scholar
  70. Savard P, Péloquin L & Sylvestre M (1986) Cloning ofPseudomonas sp. strain CBS3 genes specifying dehalogenation of 4-chlorobenzoate. J. Bacteriol. 168: 81–85Google Scholar
  71. Schmitz A, Gartemann K-H, Fiedler J, Grund E & Eichenlaub (1992) Cloning and sequence analysis of genes for dehalogenation of 4-chlorobenzoate fromArthrobacter sp. strain SU. Appl. Environ. Microbiol. 58: 4068–4071Google Scholar
  72. Schneider B, Müller R, Franck R & Lingens F (1991) Complete nucleotide sequences and comparisons of the structural genes of two 2-haloalkanoic acid dehalogenase fromPseudomonas sp. strain CBS-3. J. Bacteriol. 173: 1530–1535Google Scholar
  73. Scholten JD, Chang K-H, Babbitt PC, Charest H, Sylvestre M & Dunaway-Mariano D (1991) Novel enzymic hydrolytic dehalogenation of a chlorinated aromatic. Science 253: 182–185Google Scholar
  74. Scott-Craig JS, Panaccione DG, Pocard J-A & Walton JD (1992) The cyclic peptide synthetase catalyzing HC-toxin production in the filamentous fungusCochliobolus carbonum is encoded by a 15.7-kilobase open reading frame. J. Biol. Chem. 267: 26044–26049Google Scholar
  75. Sharma V, Suvarna K, Meganthan R & Hudspeth MES (1992) Menaquinone (Vitamin K2) biosynthesis: Nucleotide sequence and expression of themenB gene fromE. coli. J. Bacteriol. 174: 5057–5062Google Scholar
  76. Shields MS, Hooper SW & Sayler GS (1985) Plasmid-mediated mineralization of 4-chlorobiphenyl. J. Bacteriol. 163: 882–889Google Scholar
  77. Shimao M, Onishi S, Mizumori S, Kato N & Sakazawa C (1989) Degradation of 4-chlorobenzoate by facultatively alkalophilicArthrobacter sp. strain SB8. Appl. Environ. Microbiol. 55: 478–482Google Scholar
  78. Smith DJ, Earl AJ & Turner G (1990) The multifunctional peptide synthetase performing the first step of penicillin biosynthesis inPenicillin chrysogenum is a 421,073 dalton protein similar toBacillus brevis peptide antibiotic synthesis. EMBO Journal 9: 2743–2750Google Scholar
  79. Smith RF & Smith TF (1990) Automatic generation of primary sequence patterns from sets of related protein sequence. Proc. Natl. Acad. Sci. USA 87: 118-Google Scholar
  80. Staab JF, Elkins MF & Earhart CF (1989) Nucleotide sequence of theEscherichia coli entE gene. FEMS Microbiol. Lett. 59: 15–20Google Scholar
  81. Steele MI, Lorenz D, Hatter K, Park A & Sokatch JR (1992) Characterization of the mmsAB operon ofPseudomonas aeruginosa PAO encoding methylmalonate-semaldehyde dehydrogenase and 3-hydroxyisobutyrate dehydrogenase. J. Biol. Chem. 267: 13585–13592Google Scholar
  82. Suuki H, Kawarabayasi Y, Kondo J & Abe T (1990) Structure and regulation of rat long-chain acyl-CoA synthetase. J. Biol. Chem. 265: 8681–8685Google Scholar
  83. Sylvestre M, Masse R, Ayotte C, Messier T & Fauteux J (1985) Total biodegradation of 4-chlorobiphenyl (4CB) by a two membered bacterial culture. Appl. Microbiol. Biotechnol. 21: 192–195Google Scholar
  84. Tatsumi H, Kajiyama N & Nakano E (1992) Molecular cloning and expression inEscherichia coli of a cDNA clone encoding luciferase of a firefly,Luciola lateralis. Biochim. Biophys. Acta 1131: 161–165Google Scholar
  85. Thiele J, Müller R & Lingens F (1987) Initial characterization of 4-chlorobenzoate dehalogenase fromPseudomonas sp. CBS3. FEMS Microbiol. Lett. 41: 115–119Google Scholar
  86. Toh H (1990) N-Terminal halves of gramicidin 4 synthetase 1 and tyrocidine synthetase 1 as novel members of the firefly luciferase family. Protein Sequences Data Analysis 3: 512–521Google Scholar
  87. Tomioka Y, Hirose A, Moritani H, Hishinuma T, Hashimoto T & Mizugaki M (1992) cDNA cloning of mitochondrial delta-3, delta-2-enoyl-CoA isomerase of rat liver. Biochim. Biophys. Acta 1130: 109–112Google Scholar
  88. Tsoi T, Zaïtsev GM, Platnikova EG, Kosheleva IA & Boronia AM (1991) Cloning and expression ofAthrobacter globiformis 4-chlorobenzoate-4-hydroxylase inEscherichia coli. FEMS Microbiol. Lett. 81: 165–170Google Scholar
  89. Turgay K, Krause M & Marahiel MA (1992) Four homologous domains in the primary structure of GrsB are related to domains in a super-family of adenylate-forming enzymes. Mol. Microbiol. 6: 529–546Google Scholar
  90. Van Beilen JB, Eggink G, Enequist H, Box R & Witholt B (1992) DNA sequence determination and functional characterization of the OCT-plasmid-encodedalkJKL gene ofPseudomonas oleovorans. Mol. Microbiol. 6: 3121–3136Google Scholar
  91. Van den Tweel WJJ, Terburg N, Kok JB & deBont JAM (1986) Bioformation of 4-hydroxybenzoate from 4-chlorobenzoate byAlcaligenes denitrificans NTB-1. Appl. Microbiol. Biotechnol. 25: 289–294Google Scholar
  92. Weckermann R, Fuerbass R & Marahiel MA (1988) Complete nucleotide sequence of thetycA gene coding the tyrocidine synthetase 1 fromBacillus brevis. Nucleic Acids Research 16: 11841Google Scholar
  93. Weinrauch Y, Guillen N & Dubnau DA (1989) Sequence and transcription mapping ofBacillus subtilis competence genescomB andcomA, one of which is related to a family of bacterial regulatory determinants. J. Bacteriol. 171: 5362–5375Google Scholar
  94. Wohlleben W, Alijah R, Dorendorf J, Hillemann D, Nussbaumer B & Pelzer S (1992) Identification and characterization of phosphinorhricin-tripeptide biosynthetic genes inStreptomyces viridochromogenes. Gene 115: 127–132Google Scholar
  95. Wood KV, Lam YA, Seliger HH & McElroy WD (1989) Complementary DNA coding clickbeetle luciferases can elicit bioluminescence of different colors. Science (Washington, D.C.) 244: 700–702Google Scholar
  96. Yamakawa A, Nishizawa M, Fujiware KT, Kawai S, Kawasaki H, Suzuki K & Takenawa T (1991) Molecular cloning a sequencing of cDNA encoding the phosphatidylinositolkinase from rat brain. J. Biol. Chem. 266: 17850–17583Google Scholar
  97. Yura T, Mori H, Nagata T, Ishihama A, Fujita N, Iisono K, Mizobuchi K & Nakata A (1992) Systematic sequencing of theEscherichia coli genome: analysis of the 0–2.4 min region. Nucleic Acids Research 20: 3305–3308Google Scholar
  98. Zaitsev GM, Tsoi TV, Grishenkov VG, Plotnikova EG & Boronia AM (1991) Genetic control of degradation of chlorinated benzoic acids inArthrobacter globiformis, corynebacterium sepedoniuum andPseudomonas cepacia strains. FEMS Microbiol. Lett. 81: 171–176Google Scholar
  99. Zhao Y, Kung SD & Dube SK (1990) Nucleotide sequence of rice 4-coumarate: CoA ligase gene, 4-CL 1. Nucleic Acids Research 18: 6144Google Scholar

Copyright information

© Kluwer Academic Publishers 1994

Authors and Affiliations

  • Debra Dunaway-Mariano
    • 1
  • Patricia C. Babbitt
    • 2
  1. 1.Department of Chemistry and BiochemistryUniversity of MarylandCollege ParkUSA
  2. 2.Department of Pharmaceutical ChemistryUniversity of CaliforniaSan FranciscoUSA

Personalised recommendations