1887

Microbiology Society logo

Volume 152, Issue 9

Plasmids from freshwater environments capable of IncQ retrotransfer are diverse and include pQKH54, a new IncP-1 subgroup archetype Free

Abstract

Nine mercury-resistance plasmids isolated from river epilithon were assessed for their ability to retrotransfer the non-conjugative IncQ plasmid, R300B, derivatives of which have commercial uses that may result in accidental or deliberate release into the environment. Retrotransfer frequencies ranging from 2.1×10 to 1.75×10 were obtained for five of the nine plasmids – the remaining plasmids showed low or undetectable retrotransfer ability. The majority of the retrotransfer-proficient plasmids could not be classified by the tests used. Classical incompatibility testing with RP4 identified pQKH6, pQKH54 and pQM719 as IncP-1. Hybridization to replicon probes confirmed this for pQKH6 and pQM719 and added pQKH33. PCR with primers designed to amplify and regions of IncP-1 plasmids did not identify any other plasmids. Plasmids pQKH6 and pQM719 but not pQKH54 produced similar I restriction profiles to the IncP-1 subgroup. The complete nucleotide sequence of pQKH54 was determined, revealing it to have a complete IncP-1 backbone but belonging to a new distinct subgroup which was designated IncP-1. The results emphasize the ubiquity and diversity of IncP-1 plasmids in the environment but demonstrate that plasmids of as yet unknown groups are also able to retrotransfer IncQ plasmids efficiently.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
SGM
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.28941-0
2006-09-01
2024-04-25
Loading full text...

Full text loading...

/deliver/fulltext/micro/152/9/2689.html?itemId=/content/journal/micro/10.1099/mic.0.28941-0&mimeType=html&fmt=ahah

References

  1. Adamczyk M, Jagura-Burdzy G. 2003; Spread and survival of promiscuous IncP-1 plasmids. Acta Biochimica Polonica 50:425–453
     [Google Scholar]
  2. Austubel F. M, Brent R, Kingston R. E, Moore D. D, Seidman J. D, Smith J. A, Struhl K. 1989 Current Protocols in Molecular Biology New York: Wiley;
     [Google Scholar]
  3. Bale M. J, Fry J. C, Day M. J. 1987; Plasmid transfer between strains of Pseudomonas aeruginosa on membrane filters attached to river stones. J Gen Microbiol 133:3099–3107
     [Google Scholar]
  4. Bale M. J, Fry J. C, Day M. J. 1988; Transfer and occurrence of large mercury resistance plasmids in river epilithon. Appl Environ Microbiol 54:972–978
     [Google Scholar]
  5. Barkay T, Miller S. M, Summers A. O. 2003; Bacterial mercury resistance from atoms to ecosystems. FEMS Microbiol Revs 27:355–384 [CrossRef]
     [Google Scholar]
  6. Barth P. T, Grinter N. J. 1974; Comparison of the deoxyribonucleic acid molecular weights and homologies of plasmids conferring linked resistance to streptomycin and sulphonamides. J Bacteriol 120:618–630
     [Google Scholar]
  7. 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]
  8. Blanco G, Ramos F, Medina J. R, Gutierrez J. C, Tortolero M. 1991; Conjugal retrotransfer of chromosomal markers in Azotobacter vinelandii . Curr Microbiol 22:241–246 [CrossRef]
     [Google Scholar]
  9. Bolivar F, Rodriguez R. L, Greene P. J, Betlach M. C, Heyneker H. L, Boyer H. W. 1977; Construction and characterization of new cloning vehicles. II. A multipurpose cloning system. Gene 2:95–113 [CrossRef]
     [Google Scholar]
  10. Boronin A. M. 1992; Diversity of Pseudomonas plasmids: to what extent?. FEMS Microbiol Lett 100:461–468 [CrossRef]
     [Google Scholar]
  11. Bradley D. J. 1992 Gene transfer within epilithon of river stones PhD thesis UWCC; Cardiff, UK:
     [Google Scholar]
  12. Burlage R. S, Bemis L. A, Layton A. C, Sayler G. S, Larimer F. 1990; Comparative genetic organization of incompatibility group P degradative plasmids. J Bacteriol 172:6818–6825
     [Google Scholar]
  13. Couturier M, Bex F, Bergquist P. L, Maas W. K. 1988; Identification and classification of bacterial plasmids. Microbiol Rev 52:375–395
     [Google Scholar]
  14. Cross M. A, Warne S. R, Thomas C. M. 1986; Analysis of the vegetative replication origin of broad-host-range plasmid RK2 by transposon mutagenesis. Plasmid 15:132–146 [CrossRef]
     [Google Scholar]
  15. Crooks G. E, Hon G, Chandonia J. M, Brenner S. E. 2004; WebLogo: a sequence logo generator. Genome Res 14:1188–1190 which has full text at: http://weblogo.berkeley.edu//Crooks-2004-GR-WebLogo.pdf [CrossRef]
     [Google Scholar]
  16. Datta N, Hedges R. W, Shaw E. J, Sykes R. B, Richmond M. H. 1971; Properties of an R-factor from Pseudomonas aeruginosa . J Bacteriol 108:1244–1249
     [Google Scholar]
  17. Davey R. B, Bird P. I, Nikoletti S. M, Praszkier J, Pittard J. 1984; The use of mini-gal plasmids for rapid incompatibility grouping of conjugative R plasmids. Plasmid 11:234–242 [CrossRef]
     [Google Scholar]
  18. 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]
  19. Don R. H, Pemberton J. M. 1981; Properties of six pesticide degradation plasmids isolated from Alcaligenes paradoxus and Alcaligenes eutrophus . J Bacteriol 145:681–686
     [Google Scholar]
  20. Don R. H, Pemberton J. M. 1985; Genetic and physical map of the 2,4-dichlorophenoxyacetic acid degradative plasmid pJP4. J Bacteriol 161:466–468
     [Google Scholar]
  21. Droge M, Puhler A, Selbitschka W. 2000; Phenotypic and molecular characterization of conjugative antibiotic resistance plasmids isolated from bacterial communities of activated sludge. Mol Gen Genet 263:471–482 [CrossRef]
     [Google Scholar]
  22. Ewing B, Green P. 1998; Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res 8:186–194
     [Google Scholar]
  23. Ewing B, Hillier L, Wendl M. C, Green P. 1998; Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res 8:175–185 [CrossRef]
     [Google Scholar]
  24. Fry J. C, Day M. J. 1990; Plasmid transfer in the epilithon. In Bacterial Genetics in Natural Environments pp  55–80 Edited by Fry J. C., Day M. J. London: Chapman & Hall;
     [Google Scholar]
  25. Gallegos M. T, Schleif R, Bairoch A, Hofmann K, Ramos J. L. 1997; AraC/XylS family of transcriptional regulators. Microbiol Mol Biol Rev 61:393–410
     [Google Scholar]
  26. Gomis-Ruth F. X, Coll M, de la Cruz F. 2002; Structure and role of coupling proteins in conjugal DNA transfer. Res Microbiol 153:199–204 [CrossRef]
     [Google Scholar]
  27. Gordon D, Abajian C, Green P. 1998; Consed: a graphical tool for sequence finishing. Genome Res 8:195–202 [CrossRef]
     [Google Scholar]
  28. Gordon D, Desmarais C, Green P. 2001; Automated finishing with Autofinish. Genome Res 11:614–625 [CrossRef]
     [Google Scholar]
  29. Guiney D. G. 1993; Broad host range conjugative and mobilizable plasmids in Gram-negative bacteria. In Bacterial Conjugation pp  75–103 Edited by Clewell D. B. New York: Plenum;
     [Google Scholar]
  30. Hanahan D. 1983; Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166:557–580 [CrossRef]
     [Google Scholar]
  31. Hedges R. W, Matthew M. 1979; Acquisition by Escherichia coli of plasmid-borne β -lactamases normally confined to Pseudomonas spp. Plasmid 2:269–278 [CrossRef]
     [Google Scholar]
  32. Heinemann J. A, Ankenbauer R. G. 1993a; Retrotransfer in Escherichia coli conjugation: bidirectional exchange or de novo mating. J Bacteriol 175:583–588
     [Google Scholar]
  33. Heinemann J. A, Ankenbauer R. G. 1993b; Retrotransfer of IncP plasmid R751 from Escherichia coli maxicells – evidence for the genetic sufficiency of self-transferable plasmids for bacterial conjugation. Mol Microbiol 10:57–62 [CrossRef]
     [Google Scholar]
  34. Heinemann J. A, Sprague G. F. 1989; Bacterial conjugative plasmids mobilize DNA transfer between bacteria and yeast. Nature 340:205–209 [CrossRef]
     [Google Scholar]
  35. 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-1 β group without any accessory genes. Microbiology 150:3591–3599 [CrossRef]
     [Google Scholar]
  36. Hill K. E, Weightman A. J, Fry J. C. 1992; Isolation and screening of plasmids from the epilithon which mobilize recombinant plasmid pD10. Appl Environ Microbiol 58:1292–1300
     [Google Scholar]
  37. Hill K. E, Fry J. C, Weightman A. J, Day M. J, Bradley D. J, Cousland B. 1995; Retrotransfer of IncP1-like plasmids from aquatic bacteria. Lett Appl Microbiol 20:317–322 [CrossRef]
     [Google Scholar]
  38. Hooper S. W, Dockendorff T. C, Sayler G. S. 1989; Characteristics and restriction analysis of the 4-chlorobiphenyl catabolic plasmid, pSS50. Appl Environ Microbiol 55:1286–1288
     [Google Scholar]
  39. Jacob A. E. 1977; Plasmids studied in Escherichia coli and other enteric bacteria. In DNA Insertion Elements, Plasmids and Episomes pp  607–638 Edited by Bukhari A. I., Shapiro J. A., Adhya S. L. Cold Spring Habor, NY: Cold Spring Habor Laboratory;
     [Google Scholar]
  40. Jeenes D. J, Williams P. A. 1982; Excision and integration of degradative genes from TOL plasmid pWW0. J Bacteriol 150:188–194
     [Google Scholar]
  41. Jobanputra R. S, Datta N. 1974; Trimethoprim R factors in enterobacteria from clinical specimens. J Med Microbiol 7:169–177 [CrossRef]
     [Google Scholar]
  42. Kado C. I, Liu S. T. 1981; Rapid procedure for detection and isolation of large and small plasmids. J Bacteriol 145:1365–1373
     [Google Scholar]
  43. Kholodii G. Y, Yurieva O. V, Lomovskaya O. L, Gorlenko Z, Mindlin S. Z, Nikiforov V. G. 1993; Tn5053, a mercury resistance transposon with integron's ends. J Mol Biol 230:1103–1107 [CrossRef]
     [Google Scholar]
  44. Kholodii G. Y, Mindlin S. Z, Bass I. A, Yurieva O. V, Minakhina S. V, Nikiforov V. G. 1995; Four genes, two ends, and a res region are involved in transposition of Tn 5053 : a paradigm for a novel family of transposons carrying either a mer operon or an integron. Mol Microbiol 17:1189–1200 [CrossRef]
     [Google Scholar]
  45. Kittell B, Helinski D. R. 1993; Plasmid incompatibility and replication control. In Bacterial Conjugation pp  223–242 Edited by Clewell D. B. New York: Plenum;
     [Google Scholar]
  46. Kreps S, Ferino F, Mosrin C, Gerits J, Mergeay M, Thuriaux P. 1990; Conjugative transfer and autonomous replication of the promiscuous IncQ plasmid in the cyanobacterium Synechocystis PCC 6803. Mol Gen Genet 221:129–133 [CrossRef]
     [Google Scholar]
  47. Llosa M, Zunzunegui S, de la Cruz F. 2003; Conjugative coupling proteins interact with cognate and heterologous VirB10-like proteins while exhibiting specificity for cognate relaxosomes. Proc Natl Acad Sci U S A 100:10465–10470 [CrossRef]
     [Google Scholar]
  48. McClure N. C, Weightman A. J, Fry J. C. 1989; Survival of Pseudomonas putida UWC1 containing cloned catabolic genes in a model activated sludge unit. Appl Environ Microbiol 55:2627–2634
     [Google Scholar]
  49. McClure N. C, Saint C. P, Fry J. C, Weightman A. J. 1990 The Construction of Broad Host Range Genetic Markers and their Use in Monitoring the Release of Catabolic GEMS to Aquatic Environments Copenhagen, Denmark: Proceedings of the 5th European Congress on Biotechnology.;
     [Google Scholar]
  50. Mergeay M, Lejeune P, Thiry G, Faelen M. 1985; Back transfer: a property of some broad host range plasmids. In Plasmids in Bacteria p. 942 Edited by Helinski D. R., Cohen S. N., Clewell D. B., Jackson D. A., Hollaender A. New York & London: Plenum;
     [Google Scholar]
  51. Mergeay M, Lejeune P, Sadouk A, Gerits J, Fabry L. 1987; Shuttle transfer (or retrotransfer) of chromosomal markers mediated by plasmid pULB113. Mol Gen Genet 209:61–70 [CrossRef]
     [Google Scholar]
  52. Mergeay M, Springael D, Top E. 1990; Gene transfer in polluted soils. In Bacterial Genetics in Natural Environments pp  152–171 Edited by Fry J. C., Day M. J. London: Chapman & Hall;
     [Google Scholar]
  53. Norrander J, Kempe T, Messing J. 1983; Construction of improved M13 vectors using oligodeoxynucleotide-directed mutagenesis. Gene 26:101–106 [CrossRef]
     [Google Scholar]
  54. Novick R. P. 1987; Plasmid incompatibility. Microbiol Rev 51:381–395
     [Google Scholar]
  55. Osborn A. M, Bruce K. D, Strike P, Ritchie D. A. 1993; Polymerase chain reaction-restriction fragment length polymorphism analysis shows divergence among mer determinants from Gram-negative soil bacteria indistinguishable by DNA-DNA hybridization. Appl Environ Microbiol 59:4024–4030
     [Google Scholar]
  56. Pansegrau W, Lanka E, Barth P. T. & 7 other authors; 1994; Complete nucleotide sequence of Birmingham IncP-alpha plasmids – compilation and comparative analysis. J Mol Biol 239:623–663 [CrossRef]
     [Google Scholar]
  57. Perkins C. D, Davidson M. A, Day M. J, Fry J. C. 1994; Retrotransfer kinetics of R300B by pQKH6, a conjugative plasmid from river epilithon. FEMS Microbiol Ecol 15:33–44 [CrossRef]
     [Google Scholar]
  58. Powell B, Mergeay M, Christofi N. 1989; Transfer of broad host-range plasmids to sulphate-reducing bacteria. FEMS Microbiol Lett 59:269–274 [CrossRef]
     [Google Scholar]
  59. Pukall R, Tschape H, Smalla K. 1996; Monitoring the spread of broad host and narrow host range plasmids in soil microcosms. FEMS Microbiol Ecol 20:53–66 [CrossRef]
     [Google Scholar]
  60. Ramos-González M., Ramos-Díaz M., Ramos J. L. 1994; Chromosomal gene capture mediated by the Pseudomonas putida TOL catabolic plasmid. J Bacteriol 176:4635–4641
     [Google Scholar]
  61. Rhodes G, Parkhill J, Bird C, Ambrose K, Jones M. C, Huys G, Swings J, Pickup R. W. 2004; Complete nucleotide sequence of the conjugative tetracycline resistance plasmid pFBAOT6, a member of a group of IncU plasmids with global ubiquity. Appl Environ Microbiol 70:7497–7510 [CrossRef]
     [Google Scholar]
  62. Rochelle P. A, Fry J. C, Day M. J, Bale M. J. 1985; An accurate method for estimating sizes of small and large plasmids and DNA fragments by gel electrophoresis. J Gen Microbiol 132:53–59
     [Google Scholar]
  63. Rochelle P. A, Fry J. C, Day M. J. 1989; Factors affecting conjugal transfer of plasmids encoding mercury resistance from pure cultures and mixed natural suspensions of epilithic bacteria. J Gen Microbiol 135:409–424
     [Google Scholar]
  64. Ronchel M. C, Ramos-Diaz M. A, Ramos J. L. 2000; Retrotransfer of DNA in the rhizosphere. Environ Microbiol 2:319–323 [CrossRef]
     [Google Scholar]
  65. Rosenberg C, Huguet T. 1984; The pATC58 plasmid of Agrobacterium tumefaciens is not essential for tumor induction. Mol Gen Genet 196:533–536 [CrossRef]
     [Google Scholar]
  66. Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, Rajandream M.-A, Barrell B. 2000; Artemis: sequence visualisation and annotation. Bioinformatics 16:944–945 [CrossRef]
     [Google Scholar]
  67. Sambrook J, Fritsch E. F, Manniatis T. 1989 Molecular Cloning: a Laboratory Manual Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
     [Google Scholar]
  68. Schneider T. D, Stephens R. M. 1990; Sequence logos: a new way to display consensus sequences. Nucleic Acids Res 18:6097–6100 [CrossRef]
     [Google Scholar]
  69. Shah D. S, Cross M. A, Porter D, Thomas C. M. 1995; Dissection of the core and auxiliary sequences in the vegetative replication origin of promiscuous plasmid RK2. J Mol Biol 254:608–622 [CrossRef]
     [Google Scholar]
  70. Sia E. A, Kuehner D. M, Figurski D. H. 1996; Mechanism of retrotransfer in conjugation: prior transfer of the conjugative plasmid is required. J Bacteriol 178:1457–1464
     [Google Scholar]
  71. Smalla K, Krogerrecklenfort E, Heuer H. & 21 other authors; 2000; PCR-based detection of mobile genetic elements in total community DNA. Microbiology 146:1256–1257
     [Google Scholar]
  72. Smit E, Venne D, van Elsas J. D. 1993; Mobilization of a recombinant IncQ plasmid between bacteria on agar and in soil via cotransfer or retrotransfer. Appl Environ Microbiol 59:2257–2263
     [Google Scholar]
  73. Smith C. A, Thomas C. M. 1987; Comparison of the organization of the genomes of phenotypically diverse plasmids of incompatibility group-P – members of the IncP-beta-sub-group are closely related. Mol Gen Genet 206:419–427 [CrossRef]
     [Google Scholar]
  74. Smith C. A, Thomas C. M. 1989; Relationships and evolution of IncP plasmids. In Promiscuous Plasmids of Gram-negative Bacteria pp  57–77 Thomas MC. London: Academic Press;
     [Google Scholar]
  75. Smith C. A, Pinkney M, Guiney D. G, Thomas C. M. 1993; The ancestral IncP replication system consisted of contiguous oriV and trfA segments as deduced from a comparison of the nucleotide sequences of diverse IncP plasmids. J Gen Microbiol 139:1761–1766 [CrossRef]
     [Google Scholar]
  76. Stalker D. M, Thomas C. M, Helinski D. R. 1981; Nucleotide-sequence of the region of the origin of replication of the broad host range plasmid RK2. Mol Gen Genet 181:8–12 [CrossRef]
     [Google Scholar]
  77. Stanisich V. A. 1988; Identification and analysis of plasmids at the genetic level. In Plasmid Technology pp  11–47 Edited by Grinsted J., Bennett P. M. London: Academic Press;
     [Google Scholar]
  78. Szpirer C, Top E, Couturier M, Mergeay M. 1999; Retrotransfer or gene capture: a feature of conjugative plasmids, with ecological and evolutionary significance. Microbiology 145:3321–3329
     [Google Scholar]
  79. Thiry G, Mergeay M, Faelen M. 1984; Back-mobilisation of Tra[sup]−[/sup] Mob[sup]+[/sup] plasmids mediated by various IncM, IncN and IncP1 plasmids. Arch Intern Physiol Biochem 92:64–65
     [Google Scholar]
  80. Thomas C. M, Smith C. A. 1987; Incompatibility group P plasmids: genetics, evolution, and use in genetic manipulation. Annu Rev Microbiol 41:77–101 [CrossRef]
     [Google Scholar]
  81. Thomas C. M, Thorsted P. B. 1994; PCR probes for promiscuous plasmids. Microbiology 140:1
     [Google Scholar]
  82. Thomas C. M, Stalker D. M, Helinski D. R. 1981; Replication and Incompatibility properties of segments of the origin region of replication of the broad host range plasmid RK2. Mol Gen Genet 181:1–7 [CrossRef]
     [Google Scholar]
  83. Thorsted P. A, Macartney D. P, Akhtar P. & 9 other authors; 1998; Complete sequence of the IncP beta plasmid R751: implications for evolution and organisation of the IncP backbone. J Mol Biol 282:969–990 [CrossRef]
     [Google Scholar]
  84. Top E, Vanrolleghem P, Mergeay M, Verstraete W. 1992; Determination of the mechanism of retrotransfer by mechanistic mathematical modelling. J Bacteriol 174:5953–5960
     [Google Scholar]
  85. Top E, De Rore H, Collard J, Gellens V, Slobodkina G, Verstraete W, Mergeay M. 1995; Retromobilization of heavy metal resistance genes in unpolluted and heavy metal polluted soil. FEMS Microbiol Ecol 18:191–203 [CrossRef]
     [Google Scholar]
  86. Trefault N, De la Iglesia R, Molina A. M, Manzano M, Ledger T, Perez-Pantoja D, Sanchez M. A, Stuardo M, Gonzalez B. 2004; Genetic organization of the catabolic plasmid pJP4 from Ralstonia eutropha JMP134(pJP4) reveals mechanisms of adaptation to chloroaromatic pollutants and evolution of specialized chloroaromatic degradation pathways. Environ Microbiol 6:655–668 [CrossRef]
     [Google Scholar]
  87. Trieu-Cuot P, Carlier C, Martin P, Courvalin P. 1987; Plasmid transfer by conjugation from Escherichia coil to gram-positive bacteria. FEMS Microbiol Lett 48:289–294 [CrossRef]
     [Google Scholar]
  88. Vedler E. M, Vahter A, Heinaru A. 2004; The completely sequenced plasmid pEST4011 contains a novel IncP1 backbone and a catabolic transposon harbouring tfd genes for 2,4-dichlorophenoxyacetic acid degradation. J Bacteriol 186:7161–7174 [CrossRef]
     [Google Scholar]
  89. Wheatcroft R, Williams P. A. 1981; Rapid methods for the study of both stable and unstable plasmids in Pseudomonas . J Gen Microbiol 124:433–437
     [Google Scholar]
  90. Willetts N. 1981; Sites and systems for conjugal DNA transfer in bacteria. In Molecular Biology, Pathogenicity and Ecology of Bacterial Plasmids pp  207–215 Edited by Levy S. T., Clowes R. C., Koenig E. L. New York: Plenum;
     [Google Scholar]
  91. Willetts N, Crowther C. 1981; Mobilization of the non-conjugative IncQ plasmid RSF1010. Genet Res 37:311–316 [CrossRef]
     [Google Scholar]
  92. Wlodarczyk M, Piechucka E. 1995; Conjugal transfer of plasmid and chromosomal markers between strains of Thiobacillus versutus . Curr Microbiol 30:185–191 [CrossRef]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.28941-0
Loading
Plasmids from freshwater environments capable of IncQ retrotransfer are diverse and include pQKH54, a new IncP-1 subgroup archetype
Microbiology 152, 2689 (2006); https://doi.org/10.1099/mic.0.28941-0
/content/journal/micro/10.1099/mic.0.28941-0
/content/journal/micro/10.1099/mic.0.28941-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed

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