The rulB gene of plasmid pWW0 is a hotspot for the site-specific insertion of integron-like elements found in the chromosomes of environmental Pseudomonas fluorescens group bacteria

Environmental Microbiology

Volumn 16, Issue 8, 2014, Pages 2374-2388

  Rhodes, Glenn ^a   Bosma, Hester ^b   Studholme, David ^c   Arnold, Dawn L ^d   Jackson, Robert W ^e   Pickup, Roger W ^f  

^a CENTRE FOR ECOLOGY AND HYDROLOGY   (United Kingdom)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

^c UNIVERSITY OF EXETER   (United Kingdom)

^d UNIVERSITY OF THE WEST OF ENGLAND   (United Kingdom)

^e UNIVERSITY OF READING   (United Kingdom)

^f LANCASTER UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA (MICROORGANISMS); PSEUDOMONAS; PSEUDOMONAS FLUORESCENS; PSEUDOMONAS FLUORESCENS GROUP;

BACTERIAL PROTEIN; RULB PROTEIN, PSEUDOMONAS SYRINGAE;

ARTICLE; BACTERIAL CHROMOSOME; CHEMISTRY; GENETICS; GENOMIC ISLAND; INTEGRON; METABOLISM; MICROBIAL VIABILITY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; OPERON; PLASMID; PSEUDOMONAS FLUORESCENS; REPRODUCTIVE FITNESS;

BACTERIAL PROTEINS; BASE SEQUENCE; CHROMOSOMES, BACTERIAL; CONSERVED SEQUENCE; GENETIC FITNESS; GENOMIC ISLANDS; INTEGRONS; MICROBIAL VIABILITY; MOLECULAR SEQUENCE DATA; OPEN READING FRAMES; OPERON; PLASMIDS; PSEUDOMONAS FLUORESCENS;

EID: 84905367372     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12345     Document Type: Article

References (61)

1. Arnold, D.L., Jackson, R.W., Fillingham, A.J., Goss, S.C., Taylor, J.D., Mansfield, J.W., and Vivian, A. (2001) Highly conserved sequences flank avirulence genes: isolation of novel avirulence genes from Pseudomonas syringae pv. pisi. Microbiology 147: 1171-1182.
2. Baharoglu, Z., Bikard, D., and Mazel, D. (2010) Conjugative DNA transfer induces the bacterial SOS response and promotes antibiotic resistance development through integron activation. PLoS Genet 6: e1001165.
3. Baharoglu, Z., Krin, E., and Mazel, D. (2012) Connecting environment and genome plasticity in the characterization of transformation-induced SOS regulation and carbon catabolite control of the Vibrio cholerae integron integrase. J Bacteriol 194: 1659-1667.
4. Battle, S.E., Meyer, F., Rello, J., Kung, V.L., and Hauser, A.R. (2008) Hybrid pathogenicity island PAGI-5 contributes to the highly virulent phenotype of a Pseudomonas aeruginosa isolate in mammals. J Bacteriol 190: 7130-7140.
5. Böltner, D., MacMahon, C., Pembroke, J.T., Strike, P., and Osborn, A.M. (2002) R391: a conjugative integrating mosaic comprised of phage, plasmid, and transposon elements. J Bacteriol 184: 5158-5169.
6. Cambray, G., Guerout, A.-M., and Mazel, D. (2010) Integrons. Annu Rev Genet 44: 141-166.
7. Cambray, G., Sanchez-Alberola, N., Campoy, S., Guerin, É., Da Re, S., González-Zorn, B., etal. (2011) Prevalence of SOS-mediated control of integron integrase expression as an adaptive trait of chromosomal and mobile integrons. Mob DNA 2: 6.10.1186/1759-8753-2-6.
8. Cazorla, F.M., Codina, J.C., Abad, C., Arrebola, E., Tores, J.A., Murillo, J., etal. (2008) 62-kb plasmids harboring rulAB homologues confer UV-tolerance and epiphytic fitness to Pseudomonas syringae pv. syringae mango isolates. Microb Ecol 56: 283-291.
9. Dennis, J.J., and 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.
10. Dereeper, A., Guignon, V., Blanc, G., Audic, S., Buffet, S., Chevenet, F., etal. (2008) Phylogeny. fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36: W465-W469.
11. Dereeper, A., Audic, S., Claverie, J.M., and Blanc, G. (2010) BLAST-EXPLORER helps you building datasets for phylogenetic analysis. BMC Evol Biol 10: 8.
12. Franklin, F.C.H., and Williams, P.A. (1980) Construction of a partial diploid for the degradative pathway encoded by the TOL plasmid (pWW0) from Pseudomonas putida mt-2: evidence for the positive nature of the regulation by the xylR gene. Mol Gen Genet 177: 321-328.
13. Gibbon, M.J., Sesma, A., Canal, A., Wood, J.R., Hidalgo, E., Brown, J., etal. (1999) Replication regions from plant-pathogenic Pseudomonas syringae plasmids are similar to ColE2-related replicons. Microbiology 145: 325-334.
14. Greated, A., Lambertsen, L., Williams, P.A., and Thomas, C.M. (2002) Complete sequence of the IncP-9 TOL plasmid pWW0 from Pseudomonas putida. Environ Microbiol 4: 856-871.
15. Guérin, E., Jové, T., Tabesse, A., Mazel, D., and Ploy, M.-C. (2011) High-level gene cassette transcription prevents integrase expression in class 1 integrons. J Bacteriol 193: 5675-5682.
16. Guerin, É., Cambray, G., Sanchez-Alberola, N., Campoy, S., Erill, I., Da Re, S., etal. (2009) The SOS response controls integron recombination. Science 324: 1034-1034.
17. Hall, R.M. (2012) Integrons and gene cassettes: hotspots of diversity in bacterial genomes. Ann N Y Acad Sci 1267: 71-78.
18. Hochhut, B., Lotfi, Y., Mazel, D., Faruque, S.M., Woodgate, R., and Waldor, M.K. (2001) Molecular analysis of antibiotic resistance gene clusters in Vibrio cholerae O139 and O1 SXT constins. Antimicrob Agents Chemother 45: 2991-3000.
19. Jackson, R.W., Vinatzer, B., Arnold, D.L., Dorus, S., and Murillo, J. (2011) The influence of the accessory genome on bacterial pathogen evolution. Mob Genet Elements 1: 55-65.
20. Kholodii, G., Gorlenko, Z., Mindlin, S., Hobman, J., and Nikiforov, V. (2002) Tn5041-like transposons: molecular diversity, evolutionary relationships and distribution of distinct variants in environmental bacteria. Microbiology 148: 3569-3582.
21. Kivisaar, M. (2010) Mechanisms of stationary-phase mutagenesis in bacteria: mutational processes in pseudomonads. FEMS Microbiol Lett 312: 1-14.
22. Kobayashi, N., and 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.
23. Li, W., Shi, J., Wang, X., Han, Y., Tong, W., Ma, L., etal. (2004) Complete nucleotide sequence and organization of the naphthalene catabolic plasmid pND6-1 from Pseudomonas sp. strain ND6. Gene 336: 231-240.
24. Ma, Z., Smith, J.J., Zhao, Y., Jackson, R.W., Arnold, D.L., Murillo, J., and Sundin, G.W. (2007) Phylogenetic analysis of the pPT23A plasmid family of Pseudomonas syringae. Appl Environ Microbiol 73: 1287-1295.
25. Martinez, E., Marquez, C., Ingold, A., Merlino, J., Djordjevic, S.P., Stokes, H., and Chowdhury, P.R. (2012) Diverse mobilized class 1 integrons are common in the chromosomes of pathogenic Pseudomonas aeruginosa clinical isolates. Antimicrob Agents Chemother 56: 2169-2172.
26. Marttinen, P., Hanage, W.P., Croucher, N.J., Connor, T.R., Harris, S.R., Bentley, S.D., and Corander, J. (2012) Detection of recombination events in bacterial genomes from large population samples. Nucleic Acids Res 40: e6-e6.
27. Molina, L., Duque, E., Gómez, M.J., Krell, T., Lacal, J., García-Puente, A., etal. (2011) The pGRT1 plasmid of Pseudomonas putida DOT-T1E encodes functions relevant for survival under harsh conditions in the environment. Environ Microbiol 13: 2315-2327.
28. Morales-Espinosa, R., Soberón-Chávez, G., Delgado-Sapién, G., Sandner-Miranda, L., Méndez, J.L., González-Valencia, G., and Cravioto, A. (2012) Genetic and phenotypic characterization of a Pseudomonas aeruginosa Population with high frequency of genomic islands. PLoS ONE 7: e37459.
29. Morris, C.E., Glaux, C., Latour, X., Gardan, L., Samson, R., and Pitrat, M. (2000) The relationship of host range, physiology, and genotype to virulence on cantaloupe in Pseudomonas syringae from cantaloupe blight epidemics in France. Phytopathol 90: 636-646.
30. Morris, C.E., Kinkel, L.L., Xiao, K., Prior, P., and Sands, D.C. (2007) Surprising niche for the plant pathogen Pseudomonas syringae. Infect Genet Evol 7: 84-92.
31. Morris, C.E., Sands, D.C., Vinatzer, B.A., Glaux, C., Guilbaud, C., Buffière, A., etal. (2008) The life history of the plant pathogen Pseudomonas syringae is linked to the water cycle. ISME J 2: 321-334.
32. Mulet, M., Lalucat, J., and García-Valdés, E. (2010) DNA sequence-based analysis of the Pseudomonas species. Environ Microbiol 12: 1513-1530.
33. Nakazawa, T. (1978) TOL plasmid in Pseudomonas aeruginosa PAO: thermosensitivity of self-maintenance and inhibition of host cell growth. J Bacteriol 133: 527-535.
34. Ortet, P., Barakat, M., Lalaouna, D., Fochesato, S., Barbe, V., Vacherie, B., etal. (2011) Complete genome sequence of a beneficial plant root-associated bacterium, Pseudomonas brassicacearum. J Bacteriol 193: 3146-3146.
35. Patel, H.K., Da Silva, D.P., Devescovi, G., Maraite, H., Paszkiewicz, K., Studholme, D.J., and Venturi, V. (2012) Draft genome sequence of Pseudomonas fuscovaginae, a broad-host-range pathogen of plants. J Bacteriol 194: 2765-2766.
36. Pickup, R. (1989) Related plasmids found in an English Lake District stream. Microb Ecol 18: 211-220.
37. Ramírez-Díaz, M., Díaz-Magaña, A., Meza-Carmen, V., Johnstone, L., Cervantes, C., and Rensing, C. (2011) Nucleotide sequence of Pseudomonas aeruginosa conjugative plasmid pUM505 containing virulence and heavy-metal resistance genes. Plasmid 66: 7-18.
38. Ramos, J.L., Wasserfallen, A., Rose, K., and Timmis, K.N. (1987) Redesigning metabolic routes: manipulation of TOL plasmid pathway for catabolism of alkylbenzoates. Science 235: 593-596.
39. Ramos, J.L., Marqués, S., and Timmis, K.N. (1997) Transcriptional control of the Pseudomonas TOL plasmid catabolic operons is achieved through an interplay of host factors and plasmid-encoded regulators. Annu Rev Microbiol 51: 341-373.
40. Ramos-Gonzalez, M.I., Ramos-Díaz, M., and Ramos, J.L. (1994) Chromosomal gene capture mediated by the Pseudomonas putida TOL catabolic plasmid. J Bacteriol 176: 4635-4641.
41. Riffaud, C.-H., and Morris, C. (2002) Detection of Pseudomonas syringae pv. aptata in irrigation water retention basins by immunofluorescence colony-staining. Eur J Plant Pathol 108: 539-545.
42. Rodríguez-Palenzuela, P., Matas, I.M., Murillo, J., López-Solanilla, E., Bardaji, L., Pérez-Martínez, I., etal. (2010) Annotation and overview of the Pseudomonas savastanoi pv. savastanoi NCPPB 3335 draft genome reveals the virulence gene complement of a tumour-inducing pathogen of woody hosts. Environ Microbiol 12: 1604-1620.
43. Ronchel, M.C., Ramos-Díaz, M., and Ramos, J.L. (2000) Retrotransfer of DNA in the rhizosphere. Environ Microbiol 2: 319-323.
44. Roy, P.H., Tetu, S.G., Larouche, A., Elbourne, L., Tremblay, S., Ren, Q., etal. (2010) Complete genome sequence of the multiresistant taxonomic outlier Pseudomonas aeruginosa PA7. PLoS ONE 5: e8842.
45. Seth-Smith, H.M., Fookes, M.C., Okoro, C.K., Baker, S., Harris, S.R., Scott, P., etal. (2012) The SPI-7 family of integrative and conjugative elements within Enterobacteriaceae: structure, diversity and mobility. J Bacteriol 194: 1494-1504.
46. Sevastsyanovich, Y.R., Krasowiak, R., Bingle, L.E.H., Haines, A.S., Sokolov, S.L., Kosheleva, I.A., etal. (2008) Diversity of IncP-9 plasmids of Pseudomonas. Microbiology 154: 2929-2941.
47. Stavrinides, J., and Guttman, D.S. (2004) Nucleotide sequence and evolution of the five-plasmid complement of the phytopathogen Pseudomonas syringae pv. maculicola ES4326. J Bacteriol 186: 5101-5115.
48. Sundin, G.W., and Weigand, M.R. (2007) The microbiology of mutability. FEMS Microbiol Lett 277: 11-20.
49. Sundin, G.W., Kidambi, S.P., Ullrich, M., and Bender, C.L. (1996) Resistance to ultraviolet light in Pseudomonas syringae: sequence and functional analysis of the plasmid-encoded rulAB genes. Gene 177: 77-81.
50. Sundin, G.W., Jacobs, J.L., and Murillo, J. (2000) Sequence diversity of rulA among natural isolates of Pseudomonas syringae and effect on function of rulAB-mediated UV radiation tolerance. Appl Environ Microbiol 66: 5167-5173.
51. Sundin, G.W., Mayfield, C.T., Zhao, Y., Gunasekera, T.S., Foster, G.L., and Ullrich, M.S. (2004) Complete nucleotide sequence and analysis of pPSR1 (72601bp), a pPT23A-family plasmid from Pseudomonas syringae pv. syringae A2. Mol Genet Genomics 270: 462-475.
52. Tang, H., Yao, Y., Wang, L., Yu, H., Ren, Y., Wu, G., and Xu, P. (2012) Genomic analysis of Pseudomonas putida: genes in a genome island are crucial for nicotine degradation. Sci Rep 2: 377. doi:10.1038/srep00377
53. Tark, M., Tover, A., Tarassova, K., Tegova, R., Kivi, G., Horak, R., and Kivisaar, M. (2005) DNA polymerase v homologue encoded by TOL plasmid pWW0 confers evolutionary fitness on Pseudomonas putida under conditions of environmental stress. J Bacteriol 187: 5203-5213.
54. Thompson, J.D., Gibson, T., and Higgins, D.G. (2002) Multiple sequence alignment using ClustalW and ClustalX. Curr Protoc Bioinformatics 2: 3. 1-2.3. 22.
55. Untergasser, A., Cutcutache, I., Koressaar, T., Ye, J., Faircloth, B.C., Remm, M., and Rozen, S.G. (2012) Primer3 - new capabilities and interfaces. Nucleic Acids Res 40: e115-e115.
56. Winsor, G.L., Lam, D.K.W., Fleming, L., Lo, R., Whiteside, M.D., Nancy, Y.Y., etal. (2011) Pseudomonas Genome Database: improved comparative analysis and population genomics capability for Pseudomonas genomes. Nucleic Acids Res 39: D596-D600.
57. Wozniak, R.A., and Waldor, M.K. (2010) Integrative and conjugative elements: mosaic mobile genetic elements enabling dynamic lateral gene flow. Nat Rev Microbiol 8: 552-563.
58. Wozniak, R.A., Fouts, D.E., Spagnoletti, M., Colombo, M.M., Ceccarelli, D., Garriss, G., etal. (2009) Comparative ICE genomics: insights into the evolution of the SXT/R391 family of ICEs. PLoS Genet 5: e1000786.
59. Wu, D.Q., Cheng, H., Wang, C., Zhang, C., Wang, Y., Shao, J., and Duan, Q. (2012) Genome Sequence of Genomic analysis of Pseudomonas putida: genes in a genome island are crucial for nicotine degradation Strain AH16, Isolated from a Patient with Chronic Pneumonia in China. J Bacteriol 194: 5976-5977.
60. Yu, H., Yuan, M., Lu, W., Yang, J., Dai, S., Li, Q., etal. (2011) Complete genome sequence of the nitrogen-fixing and rhizosphere-associated bacterium Pseudomonas stutzeri strain DSM4166. J Bacteriol 193: 3422-3423.
61. Zhao, Y., Ma, Z., and Sundin, G.W. (2005) Comparative genomic analysis of the pPT23A plasmid family of Pseudomonas syringae. J Bacteriol 187: 2113-2126.