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PMID: 9882667 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The phn genes of Burkholderia sp. strain RP007 constitute a divergent gene cluster for polycyclic aromatic hydrocarbon catabolism.

Journal of bacteriology ·Vol. 181 ·No. 2 ·1999-01-00 ·Pages 531-40

Laurie AD, Lloyd-Jones G

Abstract

Cloning and molecular ecological studies have underestimated the diversity of polycyclic aromatic hydrocarbon (PAH) catabolic genes by emphasizing classical nah-like (nah, ndo, pah, and dox) sequences. Here we report the description of a divergent set of PAH catabolic genes, the phn genes, which although isofunctional to the classical nah-like genes, show very low homology. This phn locus, which contains nine open reading frames (ORFs), was isolated on an 11.5-kb HindIII fragment from phenanthrene-degrading Burkholderia sp. strain RP007. The phn genes are significantly different in sequence and gene order from previously characterized genes for PAH degradation. They are transcribed by RP007 when grown at the expense of either naphthalene or phenanthrene, while in Escherichia coli the recombinant phn enzymes have been shown to be capable of oxidizing both naphthalene and phenanthrene to predicted metabolites. The locus encodes iron sulfur protein alpha and beta subunits of a PAH initial dioxygenase but lacks the ferredoxin and reductase components. The dihydrodiol dehydrogenase of the RP007 pathway, PhnB, shows greater similarity to analogous dehydrogenases from described biphenyl pathways than to those characterized from naphthalene/phenanthrene pathways. An unusual extradiol dioxygenase, PhnC, shows no similarity to other extradiol dioxygenases for naphthalene or biphenyl oxidation but is the first member of the recently proposed class III extradiol dioxygenases that is specific for polycyclic arene diols. Upstream of the phn catabolic genes are two putative regulatory genes, phnR and phnS. Sequence homology suggests that phnS is a LysR-type transcriptional activator and that phnR, which is divergently transcribed with respect to phnSFECDAcAdB, is a member of the sigma54-dependent family of positive transcriptional regulators. Reverse transcriptase PCR experiments suggest that this gene cluster is coordinately expressed and is under regulatory control which may involve PhnR and PhnS.

MeSH Terms
Amino Acid Sequence Burkholderia/genetics,metabolism Cloning, Molecular Evolution, Molecular Hydrocarbons, Aromatic/metabolism Molecular Sequence Data Multigene Family Open Reading Frames Oxidoreductases/chemistry,genetics,metabolism Phenanthrenes/metabolism Phylogeny Polycyclic Compounds/metabolism Recombinant Proteins/metabolism Restriction Mapping Reverse Transcriptase Polymerase Chain Reaction Sequence Alignment Sequence Homology, Amino Acid Transcription, Genetic
Chemicals
Hydrocarbons, Aromatic Phenanthrenes Polycyclic Compounds Recombinant Proteins phenanthrene Oxidoreductases trans-1,2-dihydrobenzene-1,2-diol dehydrogenase
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Laurie A D
Department of Biological Sciences, University of Waikato, Hamilton, New Zealand.
Lloyd-Jones G
References (72)
72 references, click to expand
  1. Rapid methods for the study of both stable and unstable plasmids in Pseudomonas.
    J Gen Microbiol. 1981 Jun;124(2):433-7 PMID: 6276500
  2. Purification and propeties of (plus)-cis-naphthalene dihydrodiol dehydrogenase of Pseudomonas putida.
    J Bacteriol. 1974 Sep;119(3):879-88 PMID: 4369091
  3. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  4. Identification of a novel composite transposable element, Tn5280, carrying chlorobenzene dioxygenase genes of Pseudomonas sp. strain P51.
    J Bacteriol. 1991 Nov;173(22):7077-83 PMID: 1657878
  5. Enzyme specificity of 2-nitrotoluene 2,3-dioxygenase from Pseudomonas sp. strain JS42 is determined by the C-terminal region of the alpha subunit of the oxygenase component.
    J Bacteriol. 1998 Mar;180(5):1194-9 PMID: 9495758
  6. Cloning and nucleotide sequence of the 2,3-dihydroxybiphenyl dioxygenase gene from the PCB-degrading strain of Pseudomonas paucimobilis Q1.
    Biochemistry. 1988 May 31;27(11):3990-6 PMID: 3137968
  7. Molecular cloning of the protocatechuate 4,5-dioxygenase genes of Pseudomonas paucimobilis.
    J Bacteriol. 1990 May;172(5):2704-9 PMID: 2185230
  8. Organization and evolution of naphthalene catabolic pathways: sequence of the DNA encoding 2-hydroxychromene-2-carboxylate isomerase and trans-o-hydroxybenzylidenepyruvate hydratase-aldolase from the NAH7 plasmid.
    J Bacteriol. 1994 Dec;176(24):7757-62 PMID: 8002605
  9. Nucleotide sequences and regulational analysis of genes involved in conversion of aniline to catechol in Pseudomonas putida UCC22(pTDN1).
    J Bacteriol. 1997 Jan;179(2):399-408 PMID: 8990291
  10. Cloning of new Rhodococcus extradiol dioxygenase genes and study of their distribution in different Rhodococcus strains.
    Microbiology. 1998 Apr;144 ( Pt 4):955-63 PMID: 9579069
  11. The evolutionary relationship of biphenyl dioxygenase from gram-positive Rhodococcus globerulus P6 to multicomponent dioxygenases from gram-negative bacteria.
    Gene. 1995 Apr 14;156(1):11-8 PMID: 7737502
  12. Cloning and characterization of a chromosomal gene cluster, pah, that encodes the upper pathway for phenanthrene and naphthalene utilization by Pseudomonas putida OUS82.
    J Bacteriol. 1994 Apr;176(8):2439-43 PMID: 8157614
  13. Molecular and biochemical characterization of two meta-cleavage dioxygenases involved in biphenyl and m-xylene degradation by Beijerinckia sp. strain B1.
    J Bacteriol. 1995 Jun;177(11):3095-103 PMID: 7768806
  14. Cloning and sequencing of the genes encoding 2-nitrotoluene dioxygenase from Pseudomonas sp. JS42.
    Gene. 1996 Nov 28;181(1-2):57-61 PMID: 8973308
  15. Bacterial aromatic ring-cleavage enzymes are classified into two different gene families.
    J Biol Chem. 1989 Sep 15;264(26):15328-33 PMID: 2670937
  16. Transcriptional control of the Pseudomonas TOL plasmid catabolic operons is achieved through an interplay of host factors and plasmid-encoded regulators.
    Annu Rev Microbiol. 1997;51:341-73 PMID: 9343354
  17. 2,4-Dinitrotoluene dioxygenase from Burkholderia sp. strain DNT: similarity to naphthalene dioxygenase.
    J Bacteriol. 1996 Aug;178(16):4926-34 PMID: 8759857
  18. Molecular biology of the LysR family of transcriptional regulators.
    Annu Rev Microbiol. 1993;47:597-626 PMID: 8257110
  19. Recombination of the bph (Biphenyl) Catabolic Genes from Plasmid pWW100 and Their Deletion during Growth on Benzoate.
    Appl Environ Microbiol. 1994 Feb;60(2):691-6 PMID: 16349195
  20. Analysis of bph operon from the polychlorinated biphenyl-degrading strain of Pseudomonas pseudoalcaligenes KF707.
    J Biol Chem. 1992 Mar 5;267(7):4844-53 PMID: 1537863
  21. The Pseudomonas putida ML2 plasmid-encoded genes for benzene dioxygenase are unusual in codon usage and low in G+C content.
    Gene. 1993 Aug 16;130(1):33-9 PMID: 8344526
  22. Nucleotide sequencing and transcriptional mapping of the genes encoding biphenyl dioxygenase, a multicomponent polychlorinated-biphenyl-degrading enzyme in Pseudomonas strain LB400.
    J Bacteriol. 1992 May;174(9):2903-12 PMID: 1569021
  23. A 3-(3-hydroxyphenyl)propionic acid catabolic pathway in Rhodococcus globerulus PWD1: cloning and characterization of the hpp operon.
    J Bacteriol. 1997 Oct;179(19):6145-53 PMID: 9324265
  24. A Rhizobium tropici DNA region carrying the amino-terminal half of a nodD gene and a nod-box-like sequence confers host-range extension.
    Mol Microbiol. 1993 Sep;9(6):1157-68 PMID: 7934929
  25. Cloning of genes involved in carbazole degradation of Pseudomonas sp. strain CA10: nucleotide sequences of genes and characterization of meta-cleavage enzymes and hydrolase.
    J Bacteriol. 1997 Aug;179(15):4841-9 PMID: 9244273
  26. Purification and characterization of a 1,2-dihydroxynaphthalene dioxygenase from a bacterium that degrades naphthalenesulfonic acids.
    J Bacteriol. 1991 Jun;173(12):3795-802 PMID: 2050635
  27. Sequence and expression of the bpdC1C2BADE genes involved in the initial steps of biphenyl/chlorobiphenyl degradation by Rhodococcus sp. M5.
    Gene. 1995 Oct 16;164(1):117-22 PMID: 7590299
  28. Nucleotide sequence of the regulatory gene xylR of the TOL plasmid from Pseudomonas putida.
    Gene. 1988 Jun 30;66(2):301-6 PMID: 3169574
  29. The yields of Streptococcus faecalis grown in continuous culture.
    J Gen Microbiol. 1960 Jun;22:726-39 PMID: 14438964
  30. Microbial metabolism of polycyclic aromatic hydrocarbons.
    Adv Appl Microbiol. 1984;30:31-71 PMID: 6442534
  31. Bacterial metabolism of naphthalene: construction and use of recombinant bacteria to study ring cleavage of 1,2-dihydroxynaphthalene and subsequent reactions.
    J Bacteriol. 1992 Dec;174(23):7542-54 PMID: 1447127
  32. Catechol dioxygenases from Escherichia coli (MhpB) and Alcaligenes eutrophus (MpcI): sequence analysis and biochemical properties of a third family of extradiol dioxygenases.
    J Bacteriol. 1996 Sep;178(17):5249-56 PMID: 8752345
  33. Molecular cloning of novel genes for polycyclic aromatic hydrocarbon degradation from Comamonas testosteroni GZ39.
    Appl Environ Microbiol. 1996 Jan;62(1):230-6 PMID: 8572701
  34. The regulation of naphthalene oxygenase in pseudomonads.
    J Gen Microbiol. 1974 Jul;83(0):165-70 PMID: 4213475
  35. Identification and characterization of genes encoding carbazole 1,9a-dioxygenase in Pseudomonas sp. strain CA10.
    J Bacteriol. 1997 Aug;179(15):4850-8 PMID: 9244274
  36. A gene cluster encoding steps in conversion of naphthalene to gentisate in Pseudomonas sp. strain U2.
    J Bacteriol. 1998 May;180(9):2522-30 PMID: 9573207
  37. Nucleotide sequence of metapyrocatechase I (catechol 2,3-oxygenase I) gene mpcI from Alcaligenes eutrophus JMP222.
    Nucleic Acids Res. 1990 Jun 11;18(11):3405-6 PMID: 2356133
  38. Nitrogen fixation specific regulatory genes of Klebsiella pneumoniae and Rhizobium meliloti share homology with the general nitrogen regulatory gene ntrC of K. pneumoniae.
    Nucleic Acids Res. 1985 Jun 25;13(12):4539-55 PMID: 2989799
  39. NAH plasmid-mediated catabolism of anthracene and phenanthrene to naphthoic acids.
    Appl Environ Microbiol. 1993 Jun;59(6):1938-42 PMID: 8328810
  40. DNA sequence determination of the TOL plasmid (pWWO) xylGFJ genes of Pseudomonas putida: implications for the evolution of aromatic catabolism.
    Mol Microbiol. 1991 Oct;5(10):2459-74 PMID: 1791759
  41. p-Cumate catabolic pathway in Pseudomonas putida Fl: cloning and characterization of DNA carrying the cmt operon.
    J Bacteriol. 1996 Mar;178(5):1351-62 PMID: 8631713
  42. Studies on the isopropylbenzene 2,3-dioxygenase and the 3-isopropylcatechol 2,3-dioxygenase genes encoded by the linear plasmid of Rhodococcus erythropolis BD2.
    Microbiology. 1996 Nov;142 ( Pt 11):3241-51 PMID: 8969521
  43. Potential DNA slippage structures acquired during evolutionary divergence of Acinetobacter calcoaceticus chromosomal benABC and Pseudomonas putida TOL pWW0 plasmid xylXYZ, genes encoding benzoate dioxygenases.
    J Bacteriol. 1991 Dec;173(23):7540-8 PMID: 1938949
  44. Identification and characterization of genes encoding polycyclic aromatic hydrocarbon dioxygenase and polycyclic aromatic hydrocarbon dihydrodiol dehydrogenase in Pseudomonas putida OUS82.
    J Bacteriol. 1994 Apr;176(8):2444-9 PMID: 8157615
  45. A marine oligobacterium harboring genes known to be part of aromatic hydrocarbon degradation pathways of soil pseudomonads.
    Appl Environ Microbiol. 1996 Jun;62(6):2169-73 PMID: 8787414
  46. Expression of naphthalene oxidation genes in Escherichia coli results in the biosynthesis of indigo.
    Science. 1983 Oct 14;222(4620):167-9 PMID: 6353574
  47. Nucleotide sequencing and characterization of the genes encoding benzene oxidation enzymes of Pseudomonas putida.
    J Bacteriol. 1987 Nov;169(11):5174-9 PMID: 3667527
  48. Identification of the bphA and bphB genes of Pseudomonas sp. strains KKS102 involved in degradation of biphenyl and polychlorinated biphenyls.
    Biochem Biophys Res Commun. 1994 Jul 29;202(2):850-6 PMID: 8048958
  49. Subcloning and nucleotide sequence of the 3,4-dihydroxyphenylacetate (homoprotocatechuate) 2,3-dioxygenase gene from Escherichia coli C.
    FEBS Lett. 1990 Nov 26;275(1-2):53-7 PMID: 2261999
  50. Signal sensing by sigma 54-dependent regulators: derepression as a control mechanism.
    Mol Microbiol. 1996 Feb;19(3):409-16 PMID: 8830233
  51. Enumeration of phenanthrene-degrading bacteria by an overlayer technique and its use in evaluation of petroleum-contaminated sites.
    Appl Environ Microbiol. 1992 Aug;58(8):2579-82 PMID: 1514804
  52. Characterization of biphenyl catabolic genes of gram-positive polychlorinated biphenyl degrader Rhodococcus sp. strain RHA1.
    Appl Environ Microbiol. 1995 Jun;61(6):2079-85 PMID: 7793929
  53. Nucleotide sequences of the Acinetobacter calcoaceticus benABC genes for benzoate 1,2-dioxygenase reveal evolutionary relationships among multicomponent oxygenases.
    J Bacteriol. 1991 Sep;173(17):5385-95 PMID: 1885518
  54. Sequences of genes encoding naphthalene dioxygenase in Pseudomonas putida strains G7 and NCIB 9816-4.
    Gene. 1993 May 15;127(1):31-7 PMID: 8486285
  55. Genetic and biochemical characterization of the broad spectrum chlorobenzene dioxygenase from Burkholderia sp. strain PS12--dechlorination of 1,2,4,5-tetrachlorobenzene.
    Eur J Biochem. 1997 Jul 1;247(1):190-9 PMID: 9249026
  56. Protein measurement with the Folin phenol reagent.
    J Biol Chem. 1951 Nov;193(1):265-75 PMID: 14907713
  57. Toluene degradation by Pseudomonas putida F1. Nucleotide sequence of the todC1C2BADE genes and their expression in Escherichia coli.
    J Biol Chem. 1989 Sep 5;264(25):14940-6 PMID: 2670929
  58. Cloning and nucleotide sequence of the gene encoding the positive regulator (DmpR) of the phenol catabolic pathway encoded by pVI150 and identification of DmpR as a member of the NtrC family of transcriptional activators.
    J Bacteriol. 1993 Mar;175(6):1596-604 PMID: 8449869
  59. Oxidative metabolism of naphthalene by soil pseudomonads. The ring-fission mechanism.
    Biochem J. 1964 May;91(2):251-61 PMID: 5838388
  60. Evidence that the transcription activator encoded by the Pseudomonas putida nahR gene is evolutionarily related to the transcription activators encoded by the Rhizobium nodD genes.
    J Bacteriol. 1989 Apr;171(4):1952-9 PMID: 2703465
  61. Actions of a versatile fluorene-degrading bacterial isolate on polycyclic aromatic compounds.
    Appl Environ Microbiol. 1995 Oct;61(10):3711-23 PMID: 7487007
  62. Cloning, sequencing, and expression of isopropylbenzene degradation genes from Pseudomonas sp. strain JR1: identification of isopropylbenzene dioxygenase that mediates trichloroethene oxidation.
    Appl Environ Microbiol. 1996 Nov;62(11):3967-77 PMID: 8899984
  63. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.
    Nucleic Acids Res. 1994 Nov 11;22(22):4673-80 PMID: 7984417
  64. Aromatic effector activation of the NtrC-like transcriptional regulator PhhR limits the catabolic potential of the (methyl)phenol degradative pathway it controls.
    J Bacteriol. 1995 Mar;177(6):1485-90 PMID: 7883704
  65. Analysis of three 2,3-dihydroxybiphenyl 1,2-dioxygenases found in Rhodococcus globerulus P6. Identification of a new family of extradiol dioxygenases.
    J Biol Chem. 1994 Mar 11;269(10):7807-15 PMID: 8126007
  66. Comparative molecular analysis of genes for polycyclic aromatic hydrocarbon degradation.
    Genet Eng (N Y). 1997;19:257-69 PMID: 9193113
  67. Metabolism of dibenzothiophene and naphthalene in Pseudomonas strains: complete DNA sequence of an upper naphthalene catabolic pathway.
    J Bacteriol. 1993 Nov;175(21):6890-901 PMID: 8226631
  68. Cloning, nucleotide sequence and characterization of genes encoding naphthalene dioxygenase of Pseudomonas putida strain NCIB9816.
    Gene. 1988 Dec 20;73(2):355-62 PMID: 3243438
  69. Evolutionary relationships among extradiol dioxygenases.
    J Bacteriol. 1996 Oct;178(20):5930-7 PMID: 8830689
  70. Novel carbazole degradation genes of Sphingomonas CB3: sequence analysis, transcription, and molecular ecology.
    Biochem Biophys Res Commun. 1998 Jun 9;247(1):129-35 PMID: 9636667
  71. Genetic evidence for activation of the positive transcriptional regulator Xy1R, a member of the NtrC family of regulators, by effector binding.
    J Biol Chem. 1994 Mar 18;269(11):8059-62 PMID: 8132529
  72. Sequencing of Comamonas testosteroni strain B-356-biphenyl/chlorobiphenyl dioxygenase genes: evolutionary relationships among Gram-negative bacterial biphenyl dioxygenases.
    Gene. 1996 Oct 3;174(2):195-202 PMID: 8890734
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
1999-01-00
Pages
531-40
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC93407
Subset
IM
Databases
GENBANK
AF061751
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