1887

Abstract

sp. JF8 is a thermophilic polychlorinated biphenyl (PCB) degrader, which utilizes biphenyl and naphthalene. A thermostable, Mn-dependent 2,3-dihydroxybiphenyl 1,2-dioxygenase, BphC_JF8, has been characterized previously. Upstream of are five ORFs exhibiting low homology with, and a different gene order from, previously characterized genes. From the 5′ to 3′ direction the genes are: a putative regulatory gene (), a hydrolase (), the large and small subunits of a ring-hydroxylating dioxygenase ), and a -diol dehydrogenase (). Hybridization studies indicate that the genes are located on a plasmid. Ring-hydroxylating activity of recombinant BphA1A2_JF8 towards biphenyl, PCB, naphthalene and benzene was observed in cells, with complementation of non-specific ferredoxin and ferredoxin reductase by host cell proteins. PCB degradation by recombinant BphA1A2_JF8 showed that the congener specificity of the recombinant enzyme was similar to sp. JF8. BphD_JF8, with an optimum temperature of 85 °C, exhibited a narrow substrate preference for 2-hydroxy-6-oxo-6-phenylhexa-2,4-dienoic acid. The Arrhenius plot of BphD_JF8 was biphasic, with two characteristic energies of activation and a break point at 47 °C.

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2005-12-01
2020-01-29
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References

  1. Altschul S. F., Madden T. L., Schaffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J. 1997; Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Res25:3389–3402[CrossRef]
    [Google Scholar]
  2. Armengaud J., Happe B., Timmis K. N. 1998; Genetic analysis of dioxin dioxygenases of Sphingomonas sp. strain RW1: catabolic genes dispersed on the genome. J Bacteriol180:3954–3966
    [Google Scholar]
  3. Asturias J. A., Timmis K. N. 1993; Three different 2,3-dihydroxybiphenyl-1,2-dioxygenase genes in the gram-positive polychlorobiphenyl degrading bacterium Rhodococcus globerulus P6. J Bacteriol175:4631–4640
    [Google Scholar]
  4. Asturias J. A., Diaz E., Timmis K. N. 1995; The evolutionary relationship of biphenyl dioxygenase from gram-positive Rhodococcus globerulus P6 to multicomponent dioxygenases from gram-negative bacteria. Gene156:11–18[CrossRef]
    [Google Scholar]
  5. Barriault D., Vedadi M., Powlowski J., Sylvestre M. 1999; cis -2,3-dihydroxybiphenyl dehydrogenase and cis -1,2-dihydroxynaphthalene dehydrogenase catalyze dehydrogenation of the same range of substrates. Biochem Biophys Res Commun260:181–187[CrossRef]
    [Google Scholar]
  6. Beltrametti F., Reniero D., Backhaus S., Hofer B. 2001; Analysis of transcription of the bph locus of Burkholderia sp. strain LB400 and evidence that the ORF0 gene product acts as a regulator of the bphA1 promoter. Microbiology147:2169–2182
    [Google Scholar]
  7. Boldt Y. R., Sadowsky M. J., Ellis L. B. M., Que L., Wackett L. P Jr. 1995; A manganese-dependent dioxygenase from Arthobacter globiformis CM-2 belongs to the major extradiol dioxygenase family. J Bacteriol177:1225–1232
    [Google Scholar]
  8. Bradford M. M. 1976; A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem72:248–254[CrossRef]
    [Google Scholar]
  9. Capela D., Barloy-Hubler F., Gouzy J. & 25 other authors. 2001; Analysis of the chromosome sequence of the legume symbiont Sinorhizobium meliloti strain 1021. Proc Natl Acad Sci U S A98:9877–9882[CrossRef]
    [Google Scholar]
  10. Chen C., Taylor R. 1995; Thermophilic biodegradation of BTEX by two Thermus species. Biotechnol Bioeng48:614–624[CrossRef]
    [Google Scholar]
  11. Copley S. D. 2000; Evolution of a metabolic pathway for degradation of a toxic xenobiotic: the patchwork approach. Trends Biochem Sci25:261–265[CrossRef]
    [Google Scholar]
  12. Diaz E., Timmis K. N. 1995; Identification of functional residues in a 2-hydroxymuconic semialdehyde hydrolase. J Biol Chem270:6403–6411[CrossRef]
    [Google Scholar]
  13. Dong F.-M., Wang L.-L., Wang C.-M., Cheng J.-P., He Z.-Q., Sheng Z.-J., Shen R.-Q. 1992; Molecular cloning and mapping of phenol degradation genes from Bacillus stearothermophilus FDTP-3 and their expression in Escherichia coli . Appl Environ Microbiol58:2531–2535
    [Google Scholar]
  14. Duffner F. M., Müller R. 1998; A novel phenol hydroxylase and catechol 2,3-dioxygenase from the thermophilic Bacillus thermoleovorans strain A2: nucleotide sequence and analysis of the genes. FEMS Microbiol Lett161:37–45[CrossRef]
    [Google Scholar]
  15. Eaton R. W. 2001; Plasmid encoded phthalate catabolic pathway in Arthrobacter keyseri 12B. J Bacteriol183:3689–3703[CrossRef]
    [Google Scholar]
  16. Eaton R. W., Chapman P. J. 1992; Bacterial metabolism of naphthalene: construction and use of recombinant bacteria to study ring cleavage of 1,2-dihydroxynaphthalene and subsequent reactions. J Bacteriol174:7543–7554
    [Google Scholar]
  17. Ensley B. D., Ratzkin B. J., Osslund T. D., Simon M. J., Wackett L. P., Gibson D. T. 1983; Expression of naphthalene oxidation genes in Escherichia coli results in the biosynthsesis of indigo. Science220:167–169
    [Google Scholar]
  18. Erickson B. D., Mondello F. J. 1992; Nucleotide sequencing and transcriptional mapping of the genes encoding biphenyl dioxygenase, a multi-component polychlorinated-biphenyl-degrading enzyme in Pseudomonas strain LB400. J Bacteriol174:2903–2912
    [Google Scholar]
  19. Fujita Y., Fujita T. 1987; The gluconate operon gnt of Bacillus subtilis encodes its own transcriptional negative regulator. Proc Natl Acad Sci U S A84:4524–4528[CrossRef]
    [Google Scholar]
  20. Furukawa K., Hayase N., Taira K., Tomizuka N. 1989; Molecular relationship of chromosomal genes encoding biphenyl/polychlorinated biphenyl catabolism: some soil bacteria possess a highly conserved bph operon. J Bacteriol171:5467–5472
    [Google Scholar]
  21. Furukawa K., Hirose J., Suyama A., Zaiki T., Hayashida S. 1993; Gene components responsible for discrete substrate specificity in the metabolism of biphenyl ( bph operon) and toluene ( tod operon). J Bacteriol175:5224–5232
    [Google Scholar]
  22. Gibello A., Ferrer E., Martin M., Garrido-Pertierra A. 1994; 3,4-dihydroxyphenylacetate 2,3-dioxygenase from Klebsiella pneumoniae , a Mg2+-containing dioxygenase involved in aromatic catabolism. Biochem J301:145–150
    [Google Scholar]
  23. Gupta R. S. 1998; Protein phylogenies and signature sequence: a reappraisal of evolutionary relationships among archaebacteria, eubacteria and eukaryotes. Microbiol Mol Biol Rev62:1435–1491
    [Google Scholar]
  24. Harayama S., Kok M., Neidle E. L. 1992; Functional and evolutionary relationships among diverse oxygenases. Annu Rev Microbiol45:565–601
    [Google Scholar]
  25. Hatta T., Shimada T., Yoshihara T., Yamada A., Masai E., Fukuda M., Kiyohara H. 1998; meta -Fission product hydrolases from a strong PCB degrader Rhodococcus sp. RHA1. J Ferment Bioeng85:174–179[CrossRef]
    [Google Scholar]
  26. Hatta T., Mukerjee-Dhar G., Damborsky J., Kiyohara H., Kimbara K. 2003; Characterization of a novel thermostable Mn(II)-dependent 2,3-dihydroxybiphenyl 1,2-dioxygenase from a polychlorinated biphenyl- and naphthalene-degrading Bacillus sp. JF8. J Biol Chem278:21483–21492[CrossRef]
    [Google Scholar]
  27. Haydon D. J., Guest J. R. 1991; A new family of bacterial regulatory proteins. FEMS Microbiol Lett79:291–296[CrossRef]
    [Google Scholar]
  28. Hernaez M. J., Andujar E., Rios J. L., Kaschabek S. R., Reineke W., Santero E. 2000; Identification of a serine hydrolase which cleaves the alicyclic ring of tetralin. J Bacteriol182:5448–5453[CrossRef]
    [Google Scholar]
  29. Hofer B., Eltis L. D., Dowling D. N., Timmis K. N. 1993; Genetic analysis of a Pseudomonas locus encoding a pathway for biphenyl/polychlorinated biphenyl degrading genes. Gene 130:47–55[CrossRef]
    [Google Scholar]
  30. Hoshino T., Ikeda T., Tomizuka N., Furukawa K. 1985; Nucleotide sequence of the tetracycline resistance gene of pTHT15, a thermophilic Bacillus plasmid: comparison with staphylococcal TcR controls. Gene37:131–138[CrossRef]
    [Google Scholar]
  31. Inoue K., Widada J., Nakai S.. 9 other authors 2004; Divergent structures of carbazole degradative car operons isolated from Gram-negative bacteria. Biosci Biotechnol Biochem68:1467–1480[CrossRef]
    [Google Scholar]
  32. Ito T., Okuma K., Xue M. X., Yuzawa H., Hiramatsu K. 2003; Insights on antibiotic resistance of Staphyloccocus aureus from its whole genome: genomic island SCC. Drug Resist Updates6:41–52[CrossRef]
    [Google Scholar]
  33. Johnson J. L. 1994; Similarity analysis of DNAs. In Methods for General and Molecular Bacteriology pp655–682 Edited by Gerhardt P., Murray R. G. E., Wood W. A., Kreig N. R.. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  34. Kauppi B., Lee K., Carredano E., Parales R. E., Gibson D. T., Eklund H., Ramaswamy S. 1998; Structure of an aromatic-ring-hydroxylating dioxygenase-naphthalene 1,2-dioxygenase. Structure6:571–586[CrossRef]
    [Google Scholar]
  35. Khan A. A., Wang R.-F., Cao W.-W., Doerge D. R., Wennerstrom D., Cerniglia C. E. 2001; Molecular cloning, nucleotide sequence, and expression of genes encoding a polycyclic aromatic ring dioxygenase from Mycobacterium sp. strain PYR-1. Appl Environ Microbiol67:3577–3585[CrossRef]
    [Google Scholar]
  36. Kitagawa W., Suzuki A., Hoaki T., Masai E., Fukuda M. 2001; Multiplicity of aromatic ring hydroxylation dioxygenase genes in a strong PCB degrader, Rhodococcus sp. strain RHA1 demonstrated by denaturing gel electrophoresis. Biosci Biotechnol Biochem65:1907–1911[CrossRef]
    [Google Scholar]
  37. Knobel H.-R., Egli T., van der Meer J. R. 1996; Cloning and characterization of the genes encoding nitrilotriacetate monooxygenase of Chelatobacter heintzii ATCC 29600. J Bacteriol178:6123–6132
    [Google Scholar]
  38. Kulakov L. A., Allen C. C. R., Lipscomb D. A., Larkin M. J. 2000; Cloning and characterization of a novel cis -naphthalene dihydrodiol dehydrogenase gene ( narB ) from Rhodococcus sp. NCIMB12038. FEMS Microbiol Lett182:327–331[CrossRef]
    [Google Scholar]
  39. Kulakov L. A., Chen S., Allen C. C., Larkin M. J. 2005; Web-type evolution of Rhodococcus gene clusters associated with utilization of naphthalene. Appl Environ Microbiol71:1754–1764[CrossRef]
    [Google Scholar]
  40. Laemmli U. K. 1970; Cleavage of structural protein during assembly of the head of bacteriophage T4. Nature227:680–685[CrossRef]
    [Google Scholar]
  41. Larkin M. J., Allen C. C. R., Kulakov L. A., Lipscomb D. A. 1999; Purification and characterization of a novel naphthalene dioxygenase from Rhodococcus sp. strain NCIMB12038. J Bacteriol181:6200–6204
    [Google Scholar]
  42. Martin V. J. J., Mohn W. W. 1999; A novel aromatic-ring-hydroxylating dioxygenase from the diterpenoid-degrading bacterium Pseudomonas abietaniphila BKME-9. J Bacteriol181:2675–2682
    [Google Scholar]
  43. Masai E., Yamada A., Healy J. M., Hatta T., Kimbara K., Fukuda M. 1995; Characterization of biphenyl catabolic genes of gram-positive polychlorinated biphenyl degrader Rhodococcus sp. strain RHA1. Appl Environ Microbiol61:2079–2085
    [Google Scholar]
  44. Menn F. M., Zylstra G. J., Gibson D. T. 1991; Location and sequence of the todF gene encoding 2-hydroxy-6-oxohepta-2,4-dienoate hydrolase in Pseudomonas putida F1. Gene104:91–94[CrossRef]
    [Google Scholar]
  45. Miyazawa D., Mukerjee-Dhar G., Shimura M., Hatta T., Kimbara K. 2004; Genes for Mn(II)-dependent NahC and Fe(II)-dependent NahH located in close proximity in the thermophilic naphthalene and PCB degrader, Bacillus sp. JF8: cloning and characterization. Microbiology150:993–1004[CrossRef]
    [Google Scholar]
  46. Mouz S., Merlin C., Springael D., Toussaint A. 1999; A GntR-like negative regulator of the biphenyl degradation genes of the transposon Tn 4371 . Mol Gen Genet262:790–799[CrossRef]
    [Google Scholar]
  47. Mukerjee-Dhar G., Hatta T., Shimura M., Kimbara K. 1998; Analysis of changes in congener selectivity during PCB degradation by Burkholderia sp. strain TSN101 with increasing concentrations of PCB and characterization of the bph BCD genes and gene products. Arch Microbiol169:61–70
    [Google Scholar]
  48. Muller R. E., Ano T., Imanaka T., Aiba S. 1986; Complete nucleotide sequence of Bacillus plasmid pUB110dB, pRBH1 and its copy mutants. Mol Gen Genet202:169–171[CrossRef]
    [Google Scholar]
  49. Mutzel A., Reinscheid U. M., Antranikian G., Müller R. 1996; Isolation and characterization of a thermophilic Bacillus strain, that degrades phenol and cresols as sole carbon source at 70 °C. Appl Microbiol Biotechnol46:593–596[CrossRef]
    [Google Scholar]
  50. Nandhagopal N., Yamada A., Hatta T., Masai E., Fukuda M., Mitsui Y., Senda T. 2001; Crystal structure of 2-hydroxy-6-oxo-6-phenylhexa-2,4-dienoic acid (HPDA) hydrolase (BphD enzyme) from the Rhodococcus sp. strain RHA1 of the PCB degradation pathway. J Mol Biol309:1139–1151[CrossRef]
    [Google Scholar]
  51. Nardini M., Dijkstra B. W. 1999; α / β hydrolase fold enzymes: the family keeps growing. Curr Opin Struct Biol9:732–737[CrossRef]
    [Google Scholar]
  52. Natarajan M. R., Lu Z., Oriel P. 1994; Cloning and expression of a pathway for benzene and toluene from Bacillus stearothermophilus . Biodegradation5:77–82[CrossRef]
    [Google Scholar]
  53. Niazi J. H., Prasad D. T., Karegoudar T. B. 2001; Initial degradation of dimethylphthalate by esterases from Bacillus species. FEMS Microbiol Lett196:201–205[CrossRef]
    [Google Scholar]
  54. Ohtsubo Y., Delawary M., Kimbara K., Takagi M., Ohta A., Nagata Y. 2001; BphS, a key transcriptional regulator of the bph genes involved in polychlorinated biphenyl/biphenyl degradation in Pseudomonas sp. KKS102. J Biol Chem276:36146–36154[CrossRef]
    [Google Scholar]
  55. Page R. D. 1996; treeview: an application to display phylogenetic trees on personal computers. Comput Appl Biosci12:357–358
    [Google Scholar]
  56. Que L., Widom J., Crawford R. L. 1981; 3,4-dihydroxyphenylacetate 2,3-dioxygenase: a manganese(II) dioxygenase from Bacillus brevis . J Biol Chem256:10941–10944
    [Google Scholar]
  57. Resnick S. M., Lee K., Gibson D. T. 1996; Diverse reactions catalyzed by naphthalene dioxygenase from Pseudomonas sp. strain NCIB 9816. J Ind Microbiol17:438–457[CrossRef]
    [Google Scholar]
  58. Rigali S., Derouaux A., Giannotta F., Dusart J. 2002; Subdivision of the helix-turn-helix GntR family of bacterial regulators in FadR, HutC, MocR, and YtrA sub-families. J Biol Chem277:12507–12515[CrossRef]
    [Google Scholar]
  59. Romine M. F., Stillwell L. C., Wong K.-K., Thurston S. J., Sisk E. C., Sensen C. W., Gasterland T., Fredrickson J. K., Saffer J. D. 1998; Complete sequence of a 184-kilobase catabolic plasmid from Sphingomonas aromaticivorans strain F199. J Bacteriol181:1585–1602
    [Google Scholar]
  60. Saito A., Iwabuchi T., Harayama S. 2000; A novel phenanthrene dioxygenase from Nocardioides sp. strain KP7: expression in E. coli . J Bacteriol182:2134–2141[CrossRef]
    [Google Scholar]
  61. Saku T., Fushinobu S., Jun S.-Y., Ikeda N., Nojiri H., Yamane H., Omori T., Wakagi T. 2002; Purification, characterization and steady-state kinetics of a meta -cleavage compound hydrolase from Pseudomonas fluorescens IP01. J Biosci Bioeng93:568–574[CrossRef]
    [Google Scholar]
  62. Sambrook J., Fritsch E. F., Maniatis T. 1989; Molecular CLoning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  63. Sanger F., Nicklen S., Coulson A. R. 1977; DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A74:5463–5467[CrossRef]
    [Google Scholar]
  64. Sato S.-I., Ouchiyama N., Kimura T., Nojiri H., Yamane H., Omori T. 1997; Cloning of genes involved in carbazole degradation of Pseudomonas sp. strain CA10: nucleotide sequence of genes and characterization of meta -cleavage enzymes and hydrolase. J Bacteriol179:4841–4849
    [Google Scholar]
  65. Shimura M., Mukerjee-Dhar G., Kimbara K., Nagato H., Kiyohara H., Hatta T. 1999; Isolation and characterization of a thermophilic Bacillus sp. JF8 capable of degrading polychlorinated biphenyls and naphthalene. FEMS Microbiol Lett178:87–93[CrossRef]
    [Google Scholar]
  66. Springael D., Top E. M. 2004; Horizontal gene transfer and microbial adaptation to xenobiotics: new types of mobile genetic elements and lessons from ecological studies. Trends Microbiol12:53–58[CrossRef]
    [Google Scholar]
  67. Thompson J. D., Higgins D. G., Gibson T. J. 1994; clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res11:4673–4680
    [Google Scholar]
  68. Top E. M., Sringael D. 2003; The role of mobile elements in bacterial adaptation to xenobiotic organic compounds. Curr Opin Biotechnol14:262–269[CrossRef]
    [Google Scholar]
  69. Treadway S. L., Yanagimachi K. S., Lankenau E., Lessard P. A., Stephanopoulos G., Sinskey A. J. 1999; Isolation and characterization of indene bioconversion genes from Rhodococcus strain 124. Appl Microbiol Biotechnol51:786–793[CrossRef]
    [Google Scholar]
  70. van der Meer J. R. 1997; Evolution of novel metabolic pathways for the degradation of chloroaromatic compounds. Antonie Van Leeuwenhoek71:159–178[CrossRef]
    [Google Scholar]
  71. van der Meer J. R., de Vos W. M., Harayama S., Zehnder A. J. B. 1992; Molecular mechanisms of genetic adaptation to xenobiotic compounds. Microbiol Rev56:677–694
    [Google Scholar]
  72. Watanabe T., Inoue R., Kimura N., Furukawa K. 2000; Versatile transcription of biphenyl catabolic bph operon in Pseudomonas pseudoalcaligenes KF707. J Biol Chem275:31016–31023[CrossRef]
    [Google Scholar]
  73. Yamada A., Kishi H., Sugiyama K., Hatta T., Nakamura K., Masai E., Fukuda M. 1998; Two nearly identical aromatic compound hydrolase genes in a strong polychlorinated biphenyl degrader, Rhodococcus sp. strain RHA1. Appl Environ Microbiol64:2006–2012
    [Google Scholar]
  74. Zylstra G. J., Gibson D. T. 1989; Toluene degradation by Pseudomonas putida F1: nucleotide sequence of the todC 1 C 2 BADE genes and their expression in E. coli . J Biol Chem264:14940–14946
    [Google Scholar]
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