1887

Abstract

IncP-9 plasmids are important vehicles for degradation and resistance genes that contribute to the adaptability of species in a variety of natural habitats. The three completely sequenced IncP-9 plasmids, pWW0, pDTG1 and NAH7, show extensive homology in replication, partitioning and transfer loci (an ∼25 kb region) and to a lesser extent in the remaining backbone segments. We used PCR, DNA sequencing, hybridization and phylogenetic analyses to investigate the genetic diversity of 30 IncP-9 plasmids as well as the possibility of recombination between plasmids belonging to this family. Phylogenetic analysis of and sequences revealed nine plasmid subgroups with 7–35 % divergence between them. Only one phenotypic character was normally associated with each subgroup, except for the IncP-9 cluster, which included naphthalene- and toluene-degradation plasmids. The PCR and hybridization analysis using pWW0- and pDTG1-specific primers and probes targeting selected backbone loci showed that members of different IncP-9 subgroups have considerable similarity in their overall organization, supporting the existence of a conserved ancestral IncP-9 sequence. The results suggested that some IncP-9 plasmids are the product of recombination between plasmids of different IncP-9 subgroups but demonstrated clearly that insertion of degradative transposons has occurred on multiple occasions, indicating that association of this phenotype with these plasmids is not simply the result of divergent evolution from a single successful ancestral degradative plasmid.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2008/017939-0
2008-10-01
2019-10-14
Loading full text...

Full text loading...

/deliver/fulltext/micro/154/10/2929.html?itemId=/content/journal/micro/10.1099/mic.0.2008/017939-0&mimeType=html&fmt=ahah

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 Res 25, 3389–3402.[CrossRef]
    [Google Scholar]
  2. Antoine, R. & Locht, C. ( 1992; ). Isolation and molecular characterization of a novel broad-host-range plasmid from Bordetella bronchiseptica with sequence similarities to plasmids from Gram-positive organisms. Mol Microbiol 6, 1785–1799.[CrossRef]
    [Google Scholar]
  3. Bahl, M. I., Hansen, L. H., Goesmann, A. & Sorensen, S. J. ( 2007; ). The multiple antibiotic resistance IncP-1 plasmid pKJK5 isolated from a soil environment is phylogenetically divergent from members of the previously established α, β and δ sub-groups. Plasmid 58, 31–43.[CrossRef]
    [Google Scholar]
  4. Bayley, S. A., Morris, D. W. & Broda, P. ( 1979; ). The relationship of degradative and resistance plasmids of Pseudomonas belonging to the same incompatibility group. Nature 280, 338–339.[CrossRef]
    [Google Scholar]
  5. Birnboim, H. C. & Doly, J. ( 1979; ). A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res 7, 1513–1523.[CrossRef]
    [Google Scholar]
  6. Boronin, A. M. ( 1992; ). Diversity of Pseudomonas plasmids: to what extent? FEMS Microbiol Lett 79, 461–466.
    [Google Scholar]
  7. Boyd, E. F., Hill, C. W., Rich, S. M. & Hartl, D. L. ( 1996; ). Mosaic structure of plasmids from natural populations of Escherichia coli. Genetics 143, 1091–1100.
    [Google Scholar]
  8. Couturier, M., Bex, F., Bergquist, P. L. & Maas, W. K. ( 1988; ). Identification and classification of bacterial plasmids. Microbiol Rev 52, 375–395.
    [Google Scholar]
  9. Dahlberg, C., Linberg, C., Torsvik, V. L. & Hermansson, M. ( 1997; ). Conjugative plasmids isolated from bacteria in marine environments show various degrees of homology to each other and are not closely related to well-characterized plasmids. Appl Environ Microbiol 63, 4692–4697.
    [Google Scholar]
  10. Dennis, J. J. ( 2005; ). The evolution of IncP catabolic plasmids. Curr Opin Biotechnol 16, 291–298.[CrossRef]
    [Google Scholar]
  11. Dennis, J. J. & Zylstra, G. J. ( 2004; ). Complete sequence and genetic organization of pDTG1, the 83 kilobase naphthalene degradation plasmid from Pseudomonas putida strain NCIB 9816-4. J Mol Biol 341, 753–768.[CrossRef]
    [Google Scholar]
  12. Devereux, J., Haeberli, P. & Smithies, O. ( 1984; ). A comprehensive set of sequence-analysis programs for the VAX. Nucleic Acids Res 12, 387–395.[CrossRef]
    [Google Scholar]
  13. Dunn, N. W. & Gunsalus, I. C. ( 1973; ). Transmissible plasmid coding early enzymes of naphthalene oxidation in Pseudomonas putida. J Bacteriol 114, 974–979.
    [Google Scholar]
  14. Eaton, R. W. ( 1994; ). 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 176, 7757–7762.
    [Google Scholar]
  15. Evans, W. C., Fernley, H. N. & Griffiths, E. ( 1965; ). Oxidative metabolism of phenanthrene and anthracene by soil Pseudomonas. Biochem J 95, 819–831.
    [Google Scholar]
  16. Felsenstein, J. ( 1989; ). phylip – phylogeny inference package (version 3.2). Cladistics 5, 164–166.
    [Google Scholar]
  17. Gotz, A., Pukall, R., Smit, E., Tietze, E., Prager, R., Tschape, H., vanElsas, J. D. & Smalla, K. ( 1996; ). Detection and characterization of broad-host-range plasmids in environmental bacteria by PCR. Appl Environ Microbiol 62, 2621–2628.
    [Google Scholar]
  18. Greated, A. & Thomas, C. M. ( 1999; ). A pair of PCR primers for IncP-9 plasmids. Microbiology 145, 3003–3004.
    [Google Scholar]
  19. Greated, A., Titok, M., Krasowiak, R., Fairclough, R. J. & Thomas, C. M. ( 2000; ). The replication and stable inheritance functions of IncP-9 plasmid pM3. Microbiology 146, 2249–2258.
    [Google Scholar]
  20. Greated, A., Lambertsen, L., Williams, P. A. & Thomas, C. M. ( 2002; ). Complete sequence of the IncP-9 TOL plasmid pWW0 from Pseudomonas putida. Environ Microbiol 4, 856–871.[CrossRef]
    [Google Scholar]
  21. Haines, A. S., Akhtar, P., Jones, K., Thomas, C. M., Perkins, C. D., Williams, J. R., Day, M. J. & Fry, J. C. ( 2006; ). Plasmids from freshwater environments capable of IncQ retrotransfer are diverse and include pQKH54, a new IncP-1 subgroup archetype. Microbiology 152, 2689–2701.[CrossRef]
    [Google Scholar]
  22. Harada, K. M., Aso, Y., Hashimoto, W., Mikami, B. & Murata, K. ( 2006; ). Sequence and analysis of the 46.6-kb plasmid pA1 from Sphingomonas sp. A1 that corresponds to the typical IncP-1β plasmid backbone without any accessory gene. Plasmid 56, 11–23.[CrossRef]
    [Google Scholar]
  23. Harayama, S. & Rekik, M. ( 1989; ). Bacterial aromatic ring cleavage enzymes are classified into two different gene families. J Biol Chem 264, 15328–15333.
    [Google Scholar]
  24. Heinaru, A. L., Duggleby, C. J. & Broda, P. ( 1978; ). Molecular relationships of degradative plasmids determined by in situ hybridisation of their endonuclease-generated fragments. Mol Gen Genet 160, 347–351.[CrossRef]
    [Google Scholar]
  25. Herrick, J. B., Stuart-Keil, K. G., Ghiorse, W. C. & Madsen, E. L. ( 1997; ). Natural horizontal transfer of a naphthalene dioxygenase gene between bacteria native to a coal tar-contaminated field site. Appl Environ Microbiol 63, 2330–2337.
    [Google Scholar]
  26. Heuer, H., Szczepanowski, R., Schneiker, S., Puhler, A., Top, E. M. & Schluter, A. ( 2004; ). The complete sequences of plasmids pB2 and pB3 provide evidence for a recent ancestor of the IncP-1β group without any accessory genes. Microbiology 150, 3591–3599.[CrossRef]
    [Google Scholar]
  27. Izmalkova, T. Y., Mavrodi, D. V., Sokolov, S. L., Kosheleva, I. A., Smalla, K., Thomas, C. M. & Boronin, A. M. ( 2006; ). Molecular classification of IncP-9 naphthalene degradation plasmids. Plasmid 56, 1–10.[CrossRef]
    [Google Scholar]
  28. Jacoby, G. A. & Matthew, M. ( 1979; ). The distribution of β-lactamase genes on plasmids found in Pseudomonas. Plasmid 2, 41–47.[CrossRef]
    [Google Scholar]
  29. Kasai, Y. & Harayama, S. ( 2004; ). Catabolism of PAHs. In Pseudomonas, pp. 463–490. Edited by J.-L. Ramos. New York: Kluwer Academic/Plenum Publishers.
  30. Kawakami, Y., Mikoshiba, F., Nagasaki, S., Matsumoto, H. & Tazaki, T. ( 1972; ). Prevalence of Pseudomonas aeruginosa strains possessing R factor in hospital. J Antibiot (Tokyo) 25, 607–609.[CrossRef]
    [Google Scholar]
  31. Kobayashi, N. & Bailey, M. J. ( 1994; ). Plasmids isolated from the sugar-beet phyllosphere show little or no homology to molecular probes currently available for plasmid typing. Microbiology 140, 289–296.[CrossRef]
    [Google Scholar]
  32. Korfhagen, T. R., Sutton, L. & Jacoby, G. A. ( 1978; ). Classification and physical properties of Pseudomonas plasmids. In Microbiology-1978, pp. 221–224. Edited by D. Schlessinger. Washington, DC: American Society for Microbiology.
  33. Krasowiak, R. ( 2003; ). Analysis of elements involved in replication of pMT2 and its application for environmental screening of IncP-9 Pseudomonas plasmids. PhD thesis, University of Birmingham, UK.
  34. Krasowiak, R., Smalla, K., Sokolov, S., Kosheleva, I., Sevastyanovich, Y., Titok, M. & Thomas, C. M. ( 2002; ). PCR primers for detection and characterisation of IncP-9 plasmids. FEMS Microbiol Ecol 42, 217–225.[CrossRef]
    [Google Scholar]
  35. Lee, J. Y., Jung, K. H., Choi, S. H. & Kim, H. S. ( 1995; ). Combination of the tod and the tol pathways in redesigning a metabolic route of Pseudomonas putida for the mineralization of a benzene, toluene, and p-xylene mixture. Appl Environ Microbiol 61, 2211–2217.
    [Google Scholar]
  36. Lehrbach, P. R., McGregor, I., Ward, J. M. & Broda, P. ( 1983; ). Molecular relationships between Pseudomonas IncP-9 degradative plasmids TOL, NAH, and SAL. Plasmid 10, 164–174.[CrossRef]
    [Google Scholar]
  37. Leuchuk, A. A., Bulyha, I. M., Izmalkova, T. Y., Sevastsyanovich, Y. R., Kosheleva, I. A., Thomas, C. M. & Titok, M. A. ( 2006; ). Characterisation of Nah-plasmids of IncP-9 group from natural strains of Pseudomonas. Mol Biol 40, 750–757.[CrossRef]
    [Google Scholar]
  38. Mavrodi, D. V., Kovalenko, N. P., Sokolov, S. L., Parfeniuk, V. G., Kosheleva, I. A. & Boronin, A. M. ( 2003; ). Identification of the key genes of naphthalene catabolism in soil DNA. Mikrobiologiia 72, 672–680.
    [Google Scholar]
  39. Nüsslein, K., Maris, D., Timmis, K. & Dwyer, D. F. ( 1992; ). Expression and transfer of engineered catabolic pathways harbored by Pseudomonas spp. introduced into activated sludge microcosms. Appl Environ Microbiol 58, 3380–3386.
    [Google Scholar]
  40. Osborn, A. M., Tatley, F. M. D., Steyn, L. M., Pickup, R. W. & Saunders, J. R. ( 2000; ). Mosaic plasmids and mosaic replicons: evolutionary lessons from the analysis of genetic diversity in IncFII-related replicons. Microbiology 146, 2267–2275.
    [Google Scholar]
  41. Page, R. D. M. ( 1996; ). TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12, 357–358.
    [Google Scholar]
  42. Panke, S., Sanchez-Romero, J. M. & de Lorenzo, V. ( 1998; ). Engineering of quasi-natural Pseudomonas putida strains for toluene metabolism through an ortho-cleavage degradation pathway. Appl Environ Microbiol 64, 748–751.
    [Google Scholar]
  43. Parales, R. E., Bruce, N. C., Schmid, A. & Wackett, L. P. ( 2002; ). Biodegradation, biotransformation, and biocatalysis (B3). Appl Environ Microbiol 68, 4699–4709.[CrossRef]
    [Google Scholar]
  44. Ramos, J. L. & Timmis, K. N. ( 1987; ). Experimental evolution of catabolic pathways of bacteria. Microbiol Sci 4, 228–237.
    [Google Scholar]
  45. Ramos, J. L., Wasserfallen, A., Rose, K. & Timmis, K. N. ( 1987; ). Redesigning metabolic routes: manipulation of TOL plasmid pathway for catabolism of alkylbenzoates. Science 235, 593–596.[CrossRef]
    [Google Scholar]
  46. Ramos, J. L., Marques, S. & Timmis, K. N. ( 1997; ). Transcriptional control of the Pseudomonas TOL plasmid catabolic operons is achieved through interplay of host factors and plasmid-encoded regulators. Annu Rev Microbiol 51, 341–373.[CrossRef]
    [Google Scholar]
  47. Rawlings, D. E. ( 2005; ). The evolution of pTF-FC2 and pTC-F14, two related plasmids of the IncQ-family. Plasmid 53, 137–147.[CrossRef]
    [Google Scholar]
  48. Rawlings, D. E. & Tietze, E. ( 2001; ). Comparative biology of IncQ and IncQ-like plasmids. Microbiol Mol Biol Rev 65, 481–496.[CrossRef]
    [Google Scholar]
  49. Rutherford, K., Parkhill, J., Crook, J., Horsnell, T., Rice, P., Rajandream, M. A. & Barrel, B. ( 2000; ). Artemis: sequence visualization and annotation. Bioinformatics 16, 944–945.[CrossRef]
    [Google Scholar]
  50. Saitou, N. & Nei, M. ( 1987; ). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4, 406–425.
    [Google Scholar]
  51. Sambrook, J. & Russell, D. W. ( 2001; ). Molecular Cloning: a Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  52. Schluter, A., Heuer, H., Szczepanowski, R., Forney, L. J., Thomas, C. M., Puhler, A. & Top, E. M. ( 2003; ). The 64 508 bp IncP-1β antibiotic multiresistance plasmid pB10 isolated from a waste-water treatment plant provides evidence for recombination between members of different branches of the IncP-1β group. Microbiology 149, 3139–3153.[CrossRef]
    [Google Scholar]
  53. Sentchilo, V. S., Perebituk, A. N., Zehnder, A. J. B. & van der Meer, J. R. ( 2000; ). Molecular diversity of plasmids bearing genes that encode toluene and xylene metabolism in Pseudomonas strains isolated from different contaminated sites in Belarus. Appl Environ Microbiol 66, 2842–2852.[CrossRef]
    [Google Scholar]
  54. Smalla, K., Krogerrecklenfort, E., Heuer, H., Dejonghe, W., Top, E., Osborn, M., Niewint, J., Tebbe, C., Barr, M. & other authors ( 2000; ). PCR-based detection of mobile genetic elements in total community DNA. Microbiology 146, 1256–1257.
    [Google Scholar]
  55. Sobecky, P. A., Mincer, T. J., Chang, M. C. & Helinski, D. R. ( 1997; ). Plasmids isolated from marine sediment microbial communities contain replication and incompatibility regions unrelated to those of known plasmid groups. Appl Environ Microbiol 63, 888–895.
    [Google Scholar]
  56. Sota, M., Yano, H., Ono, A., Miyazaki, R., Ishii, H., Genka, H., Top, E. M. & Tsuda, M. ( 2006; ). Genomic and functional analysis of the IncP-9 naphthalene-catabolic plasmid NAH7 and its transposon Tn4655 suggests catabolic gene spread by a tyrosine recombinase. J Bacteriol 188, 4057–4067.[CrossRef]
    [Google Scholar]
  57. Tamura, K., Dudley, J., Nei, M. & Kumar, S. ( 2007; ). MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24, 1596–1599.[CrossRef]
    [Google Scholar]
  58. Tan, H. M. ( 1999; ). Bacterial catabolic transposons. Appl Microbiol Biotechnol 51, 1–12.[CrossRef]
    [Google Scholar]
  59. Thomas, C. M. ( 2000a; ). The Horizontal Gene Pool. Amsterdam: Harwood Academic Publishers.
  60. Thomas, C. M. ( 2000b; ). Paradigms of plasmid organization. Mol Microbiol 37, 485–491.
    [Google Scholar]
  61. Thomas, C. M. & Haines, A. S. ( 2004; ). Plasmids of the genus Pseudomonas. In Pseudomonas, pp. 197–231. Edited by J.-L. Ramos. London: Kluwer/Plenum.
  62. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. & Higgins, D. G. ( 1997; ). The clustal_x windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25, 4876–4882.[CrossRef]
    [Google Scholar]
  63. Titok, M. A., Maksimova, N. P. & Fomichev, Y. K. ( 1991; ). Characteristics of the broad host range IncP-9 plasmid pM3. Mol Genet Microbiol Virol 8, 18–23.
    [Google Scholar]
  64. Top, E. M., Springael, D. & Boon, N. ( 2002; ). Catabolic mobile genetic elements and their potential use in bioaugmentation of polluted soils and waters. FEMS Microbiol Ecol 42, 199–208.[CrossRef]
    [Google Scholar]
  65. Toussaint, A. & Merlin, C. ( 2002; ). Mobile elements as a combination of functional modules. Plasmid 47, 26–35.[CrossRef]
    [Google Scholar]
  66. Tsuda, M., Tan, H. M., Nishi, A. & Furukawa, K. ( 1999; ). Mobile catabolic genes in bacteria. J Biosci Bioeng 87, 401–410.[CrossRef]
    [Google Scholar]
  67. Turner, S. L., Bailey, M. J., Lilley, A. K. & Thomas, C. M. ( 2002; ). Ecological and molecular maintenance strategies of mobile genetic elements. FEMS Microbiol Ecol 42, 177–185.[CrossRef]
    [Google Scholar]
  68. Vedler, E., Vahter, M. & Heinaru, A. ( 2004; ). The completely sequenced plasmid pEST4011 contains a novel IncP1 backbone and a catabolic transposon harboring tfd genes for 2,4-dichlorophenoxyacetic acid degradation. J Bacteriol 186, 7161–7174.[CrossRef]
    [Google Scholar]
  69. Wackett, L. P. ( 2003; ). Pseudomonas putida – a versatile biocatalyst. Nat Biotechnol 21, 136–138.[CrossRef]
    [Google Scholar]
  70. Williams, P. A. & Murray, K. ( 1974; ). Metabolism of benzoate and the methylbenzoates by Pseudomonas putida (arvilla) mt-2: evidence of the existence of TOL plasmid. J Bacteriol 120, 416–423.
    [Google Scholar]
  71. Yen, K. M. & Gunsalus, I. C. ( 1982; ). Plasmid gene organization: naphthalene/salicylate oxidation. Proc Natl Acad Sci U S A 79, 874–878.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2008/017939-0
Loading
/content/journal/micro/10.1099/mic.0.2008/017939-0
Loading

Data & Media loading...

[PDF file](56 KB)

PDF

[PDF file](98 KB)

PDF

[PDF file](43 KB)

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error