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PMID: 12676698 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Horizontal transfer of phnAc dioxygenase genes within one of two phenotypically and genotypically distinctive naphthalene-degrading guilds from adjacent soil environments.

Applied and environmental microbiology ·Vol. 69 ·No. 4 ·2003-04-00 ·Pages 2172-81

Wilson MS, Herrick JB, Jeon CO, Hinman DE, Madsen EL

Abstract

Several distinct naphthalene dioxygenases have been characterized to date, which provides the opportunity to investigate the ecological significance, relative distribution, and transmission modes of the different analogs. In this study, we showed that a group of naphthalene-degrading isolates from a polycyclic aromatic hydrocarbon (PAH)-contaminated hillside soil were phenotypically and genotypically distinct from naphthalene-degrading organisms isolated from adjacent, more highly contaminated seep sediments. Mineralization of (14)C-labeled naphthalene by soil slurries suggested that the in situ seep community was more acclimated to PAHs than was the in situ hillside community. phnAc-like genes were present in diverse naphthalene-degrading isolates cultured from the hillside soil, while nahAc-like genes were found only among isolates cultured from the seep sediments. The presence of a highly conserved nahAc allele among gram-negative isolates from the coal tar-contaminated seep area provided evidence for in situ horizontal gene transfer and was reported previously (J. B. Herrick, K. G. Stuart-Keil, W. C. Ghiorse, and E. L. Madsen, Appl. Environ. Microbiol. 63:2330-2337, 1997). Natural horizontal transfer of the phnAc sequence was also suggested by a comparison of the phnAc and 16S ribosomal DNA sequences of the hillside isolates. Analysis of metabolites produced by cell suspensions and patterns of amplicons produced by PCR analysis suggested both genetic and metabolic diversity among the naphthalene-degrading isolates of the contaminated hillside. These results provide new insights into the distribution, diversity, and transfer of phnAc alleles and increase our understanding of the acclimation of microbial communities to pollutants.

MeSH Terms
Bacteria/classification,enzymology,genetics Biodegradation, Environmental Burkholderia/classification,enzymology,genetics Coal Tar/metabolism Dioxygenases Gene Transfer, Horizontal Genotype Molecular Sequence Data Multienzyme Complexes/genetics,metabolism Naphthalenes/metabolism Oxygenases/genetics,metabolism Phenanthrenes/metabolism Phenotype Pseudomonas/classification,enzymology,genetics RNA, Ribosomal, 16S/genetics Sequence Analysis, DNA Soil Microbiology Soil Pollutants/metabolism
Chemicals
Multienzyme Complexes Naphthalenes Phenanthrenes RNA, Ribosomal, 16S Soil Pollutants naphthalene phenanthrene Coal Tar Oxygenases Dioxygenases naphthalene dioxygenase
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Wilson Mark S
Department of Biology, Humboldt State University, Arcata, California 95521, USA.
Herrick James B
Jeon Che Ok
Hinman David E
Madsen Eugene L
References (57)
57 references, click to expand
  1. In situ, real-time catabolic gene expression: extraction and characterization of naphthalene dioxygenase mRNA transcripts from groundwater.
    Appl Environ Microbiol. 1999 Jan;65(1):80-7 PMID: 9872763
  2. Genetics of naphthalene and phenanthrene degradation by Comamonas testosteroni.
    J Ind Microbiol Biotechnol. 1997 Nov-Dec;19(5-6):401-7 PMID: 9451837
  3. Functional and evolutionary relationships among diverse oxygenases.
    Annu Rev Microbiol. 1992;46:565-601 PMID: 1444267
  4. Evaluation of strains isolated by growth on naphthalene and biphenyl for hybridization of genes to dioxygenase probes and polychlorinated biphenyl-degrading ability.
    Appl Environ Microbiol. 1996 Jun;62(6):2053-8 PMID: 8787402
  5. Structure of an aromatic-ring-hydroxylating dioxygenase-naphthalene 1,2-dioxygenase.
    Structure. 1998 May 15;6(5):571-86 PMID: 9634695
  6. Quantification of phnAc and nahAc in contaminated new zealand soils by competitive PCR.
    Appl Environ Microbiol. 2000 May;66(5):1814-7 PMID: 10788344
  7. The evolution of pathways for aromatic hydrocarbon oxidation in Pseudomonas.
    Biodegradation. 1994 Dec;5(3-4):195-217 PMID: 7765833
  8. Isolation and characterization of polycyclic aromatic hydrocarbon-degrading bacteria associated with the rhizosphere of salt marsh plants.
    Appl Environ Microbiol. 2001 Jun;67(6):2683-91 PMID: 11375181
  9. Evolution of a pathway for chlorobenzene metabolism leads to natural attenuation in contaminated groundwater
    Appl Environ Microbiol. 1998 Nov;64(11):4185-93 PMID: 9797264
  10. Natural horizontal transfer of a naphthalene dioxygenase gene between bacteria native to a coal tar-contaminated field site.
    Appl Environ Microbiol. 1997 Jun;63(6):2330-7 PMID: 9172352
  11. Culture-based and non-growth-dependent detection of the Burkholderia cepacia complex in soil environments.
    Appl Environ Microbiol. 2002 Aug;68(8):3750-8 PMID: 12147469
  12. Isolation and characterization of indene bioconversion genes from Rhodococcus strain I24.
    Appl Microbiol Biotechnol. 1999 Jun;51(6):786-93 PMID: 10422226
  13. Evidence for aromatic ring reduction in the biodegradation pathway of carboxylated naphthalene by a sulfate reducing consortium.
    Biodegradation. 2000;11(2-3):117-24 PMID: 11440239
  14. Selection of specific endophytic bacterial genotypes by plants in response to soil contamination.
    Appl Environ Microbiol. 2001 Jun;67(6):2469-75 PMID: 11375152
  15. Detection of polycyclic aromatic hydrocarbon degradation genes in different soil bacteria by polymerase chain reaction and DNA hybridization.
    FEMS Microbiol Lett. 1999 Apr 1;173(1):255-63 PMID: 10220903
  16. The phn genes of Burkholderia sp. strain RP007 constitute a divergent gene cluster for polycyclic aromatic hydrocarbon catabolism.
    J Bacteriol. 1999 Jan;181(2):531-40 PMID: 9882667
  17. 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
  18. 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
  19. 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. 1994 Apr;60(4):1106-15 PMID: 8017907
  20. Insights into the genetic diversity of initial dioxygenases from PAH-degrading bacteria.
    Appl Microbiol Biotechnol. 2001 May;55(5):609-18 PMID: 11414329
  21. In situ biodegradation: microbiological patterns in a contaminated aquifer.
    Science. 1991 May 10;252(5007):830-3 PMID: 2028258
  22. Substrate specificities of hybrid naphthalene and 2,4-dinitrotoluene dioxygenase enzyme systems.
    J Bacteriol. 1998 May;180(9):2337-44 PMID: 9573183
  23. 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
  24. Naphthalene and donor cell density influence field conjugation of naphthalene catabolism plasmids.
    Appl Environ Microbiol. 2000 Jul;66(7):3088-92 PMID: 10877811
  25. Hybridization of nucleic acids immobilized on solid supports.
    Anal Biochem. 1984 May 1;138(2):267-84 PMID: 6204550
  26. Detection of genes for alkane and naphthalene catabolism in Rhodococcus sp. strain 1BN.
    Environ Microbiol. 2000 Oct;2(5):572-7 PMID: 11233165
  27. Stereochemistry and evidence for an arene oxide-NIH shift pathway in the fungal metabolism of naphthalene.
    Chem Biol Interact. 1983 Apr-May;44(1-2):119-32 PMID: 6406078
  28. Pseudomonas classification. A new case history in the taxonomy of gram-negative bacteria.
    Antonie Van Leeuwenhoek. 1993-1994;64(3-4):231-51 PMID: 8085787
  29. Polymerase chain reaction amplification of naphthalene-catabolic and 16S rRNA gene sequences from indigenous sediment bacteria.
    Appl Environ Microbiol. 1993 Mar;59(3):687-94 PMID: 7683182
  30. Genetic characterization and evolutionary implications of a chromosomally encoded naphthalene-degradation upper pathway from Pseudomonas stutzeri AN10.
    Gene. 1999 Aug 5;236(1):149-57 PMID: 10433976
  31. Initial reactions in the oxidation of naphthalene by Pseudomonas putida.
    Biochemistry. 1975 Feb 11;14(3):575-84 PMID: 234247
  32. The aerobic pseudomonads: a taxonomic study.
    J Gen Microbiol. 1966 May;43(2):159-271 PMID: 5963505
  33. 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
  34. Multiplicity of aromatic ring hydroxylation dioxygenase genes in a strong PCB degrader, Rhodococcus sp. strain RHA1 demonstrated by denaturing gradient gel electrophoresis.
    Biosci Biotechnol Biochem. 2001 Aug;65(8):1907-11 PMID: 11577742
  35. Purification and characterization of a novel naphthalene dioxygenase from Rhodococcus sp. strain NCIMB12038.
    J Bacteriol. 1999 Oct;181(19):6200-4 PMID: 10498739
  36. Effect of 2-hydroxybenzoate on the maintenance of naphthalene-degrading pseudomonads in seeded and unseeded soil.
    Appl Environ Microbiol. 1991 Oct;57(10):2873-9 PMID: 1746947
  37. Differential detection of key enzymes of polyaromatic-hydrocarbon-degrading bacteria using PCR and gene probes.
    Microbiology. 1999 Jul;145 ( Pt 7):1731-41 PMID: 10439412
  38. Polycyclic aromatic hydrocarbon degradation by a new marine bacterium, Neptunomonas naphthovorans gen. nov., sp. nov.
    Appl Environ Microbiol. 1999 Jan;65(1):251-9 PMID: 9872786
  39. The RDP-II (Ribosomal Database Project).
    Nucleic Acids Res. 2001 Jan 1;29(1):173-4 PMID: 11125082
  40. Molecular detection and diversity of polycyclic aromatic hydrocarbon-degrading bacteria isolated from geographically diverse sites.
    Appl Microbiol Biotechnol. 2002 Feb;58(2):202-9 PMID: 11876413
  41. 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
  42. Isolation of marine polycyclic aromatic hydrocarbon (PAH)-degrading Cycloclasticus strains from the Gulf of Mexico and comparison of their PAH degradation ability with that of puget sound Cycloclasticus strains.
    Appl Environ Microbiol. 1998 Dec;64(12):4703-10 PMID: 9835552
  43. Aromatic hydrocarbon dioxygenases in environmental biotechnology.
    Curr Opin Biotechnol. 2000 Jun;11(3):236-43 PMID: 10851146
  44. Engineering bacteria for bioremediation.
    Curr Opin Biotechnol. 2000 Jun;11(3):262-70 PMID: 10851148
  45. Microbial ecology of the terrestrial subsurface.
    Adv Appl Microbiol. 1988;33:107-72 PMID: 3041739
  46. Catabolic plasmids of environmental and ecological significance.
    Microb Ecol. 1990 Jan;19(1):1-20 PMID: 24196251
  47. Burkholderia graminis sp. nov., a rhizospheric Burkholderia species, and reassessment of [Pseudomonas] phenazinium, [Pseudomonas] pyrrocinia and [Pseudomonas] glathei as Burkholderia.
    Int J Syst Bacteriol. 1998 Apr;48 Pt 2:549-63 PMID: 9731297
  48. Geochemical and physiological evidence for mixed aerobic and anaerobic field biodegradation of coal tar waste by subsurface microbial communities.
    Microb Ecol. 2002 Aug;44(2):107-17 PMID: 12087424
  49. Spatial and temporal variation of phenanthrene-degrading bacteria in intertidal sediments.
    Appl Environ Microbiol. 1998 Jul;64(7):2560-5 PMID: 9647830
  50. Molecular cloning, nucleotide sequence, and expression of genes encoding a polycyclic aromatic ring dioxygenase from Mycobacterium sp. strain PYR-1.
    Appl Environ Microbiol. 2001 Aug;67(8):3577-85 PMID: 11472934
  51. Oxidative metabolism of naphthalene by soil pseudomonads. The ring-fission mechanism.
    Biochem J. 1964 May;91(2):251-61 PMID: 5838388
  52. Quantitative cell lysis of indigenous microorganisms and rapid extraction of microbial DNA from sediment.
    Appl Environ Microbiol. 1994 May;60(5):1572-80 PMID: 8017936
  53. Trichloroethylene degradation by Escherichia coli containing the cloned Pseudomonas putida F1 toluene dioxygenase genes.
    Appl Environ Microbiol. 1989 Dec;55(12):3162-6 PMID: 2694960
  54. Horizontal gene transfer in prokaryotes: quantification and classification.
    Annu Rev Microbiol. 2001;55:709-42 PMID: 11544372
  55. 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
  56. Plasmids responsible for horizontal transfer of naphthalene catabolism genes between bacteria at a coal tar-contaminated site are homologous to pDTG1 from pseudomonas putida NCIB 9816-4
    Appl Environ Microbiol. 1998 Oct;64(10):3633-40 PMID: 9758778
  57. Molecular mechanisms of genetic adaptation to xenobiotic compounds.
    Microbiol Rev. 1992 Dec;56(4):677-94 PMID: 1480115
Article Info
Journal
Applied and environmental microbiology
Abbr.
Appl Environ Microbiol
ISSN
0099-2240
Published
2003-04-00
Pages
2172-81
Language
English
Region
United States
NLM ID
7605801
PMCID
PMC154808
Subset
IM
Databases
GENBANK
AY154358, AY154359, AY154360, AY154361, AY154362, AY154363, AY154364, AY154365, AY154366, AY154367, AY154368, AY154369, AY154370, AY154371, AY154372, AY154373, AY154374, AY154375, AY154376, AY154377, AY154378, AY154379
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