1887

Microbiology Society logo

Volume 150, Issue 11

Antibiotic multiresistance plasmid pRSB101 isolated from a wastewater treatment plant is related to plasmids residing in phytopathogenic bacteria and carries eight different resistance determinants including a multidrug transport system Free

Abstract

Ten different antibiotic resistance plasmids conferring high-level erythromycin resistance were isolated from an activated sludge bacterial community of a wastewater treatment plant by applying a transformation-based approach. One of these plasmids, designated pRSB101, mediates resistance to tetracycline, erythromycin, roxythromycin, sulfonamides, cephalosporins, spectinomycin, streptomycin, trimethoprim, nalidixic acid and low concentrations of norfloxacin. Plasmid pRSB101 was completely sequenced and annotated. Its size is 47 829 bp. Conserved synteny exists between the pRSB101 replication/partition (/) module and the pXAC33-replicon from the phytopathogen pv. . The second pRSB101 backbone module encodes a three-Mob-protein type mobilization () system with homology to that of IncQ-like plasmids. Plasmid pRSB101 is mobilizable with the help of the IncP-1 plasmid RP4 providing transfer functions . A 20 kb resistance region on pRSB101 is located within an integron-containing Tn-like transposon. The variable region of the class 1 integron carries the genes for a dihydrofolate reductase, for a spectinomycin/streptomycin adenylyltransferase and for a so far unknown Ambler class A extended spectrum -lactamase. The integron-specific 3′-segment (ΔΔ) is connected to a macrolide resistance operon consisting of the genes (A) (macrolide 2′-phosphotransferase I), (hydrophobic protein of unknown function) and (A) (regulatory protein). Finally, a putative mobile element with the tetracycline resistance genes (tetracycline efflux pump) and was identified upstream of the Tn-specific transposase gene . The second ‘genetic load’ region on pRSB101 harbours four distinct mobile genetic elements, another integron belonging to a new class and footprints of two more transposable elements. A tripartite multidrug (MDR) transporter consisting of an ATP-binding-cassette (ABC)-type ATPase and permease, and an efflux membrane fusion protein (MFP) of the RND-family is encoded between the replication/partition and the mobilization module. Homologues of the macrolide resistance genes (A), and (A) were detected on eight other erythromycin resistance-plasmids isolated from activated sludge bacteria. Plasmid pRSB101-like amplicons were also obtained from plasmid-DNA preparations of the final effluents of the wastewater treatment plant indicating that pRSB101-like plasmids are released with the final effluents into the environment.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): DR, direct repeat , Inc, incompatibility , MDR, multidrug resistance , MFP, membrane fusion protein , OMF, outer-membrane factor and RND, resistance nodulation division
SGM
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.27317-0
2004-11-01
2024-04-16
Loading full text...

Full text loading...

/deliver/fulltext/micro/150/11/mic1503613.html?itemId=/content/journal/micro/10.1099/mic.0.27317-0&mimeType=html&fmt=ahah

References

  1. Adamczyk M., Jagura-Burdzy G. 2003; Spread and survival of promiscuous IncP-1 plasmids. Acta Biochim Pol 50:425–453
     [Google Scholar]
  2. Aminov R. I., Chee-Sanford J. C., Garrigues N., Teferedegne B., Krapac I. J., White B. A., Mackie R. I. 2002; Development, validation, and application of PCR primers for detection of tetracycline efflux genes of Gram-negative bacteria. Appl Environ Microbiol 68:1786–1793 [CrossRef]
     [Google Scholar]
  3. Artiguenave F., Vilagines R., Danglot C. 1997; High-efficiency transposon mutagenesis by electroporation of a Pseudomonas fluorescens strain. FEMS Microbiol Lett 153:363–369 [CrossRef]
     [Google Scholar]
  4. Bateman A., Coin L., Durbin R. 10 other authors 2004; The Pfam protein families database. Nucleic Acids Res 32: database issue: D138–D141 [CrossRef]
     [Google Scholar]
  5. Bennett P. M. 1999; Integrons and gene cassettes: a genetic construction kit for bacteria. J Antimicrob Chemother 43:1–4
     [Google Scholar]
  6. Bissonnette L., Roy P. H. 1992; Characterization of In0 of Pseudomonas aeruginosa plasmid pVS1, an ancestor of integrons of multiresistance plasmids and transposons of gram-negative bacteria. J Bacteriol 174:1248–1257
     [Google Scholar]
  7. Blázquez J., Navas A., Gonzalo P., Martinez J. L., Baquero F. 1996; Spread and evolution of natural plasmids harboring transposon Tn5. FEMS Microbiol Ecol 19:63–71 [CrossRef]
     [Google Scholar]
  8. Blondeau J. M. 2002; The evolution and role of macrolides in infectious diseases. Expert Opin Pharmacother 3:1131–1151 [CrossRef]
     [Google Scholar]
  9. Blondeau J. M., DeCarolis E., Metzler K. L., Hansen G. T. 2002; The macrolides. Expert Opin Investig Drugs 11:189–215 [CrossRef]
     [Google Scholar]
  10. Buckle A. M., Schreiber G., Fersht A. R. 1994; Protein-protein recognition: crystal structural analysis of a barnase-barstar complex at 2·0-Å resolution. Biochemistry 33:8878–8889 [CrossRef]
     [Google Scholar]
  11. Burse A., Weingart H., Ullrich M. S. 2004; The phytoalexin-inducible multidrug efflux pump AcrAB contributes to virulence in the fire blight pathogen, Erwinia amylovora . Mol Plant–Microbe Interact 17:43–54 [CrossRef]
     [Google Scholar]
  12. Chopra I., Roberts M. 2001; Tetracycline antibiotics: mode of action, applications, molecular biology, and epidemiology of bacterial resistance. Microbiol Mol Biol Rev 65:232–260 [CrossRef]
     [Google Scholar]
  13. Cooksey D. A. 1990; Genetics of bactericide resistance in plant pathogenic bacteria. Annu Rev Phytopathol 28:201–219 [CrossRef]
     [Google Scholar]
  14. da Silva A. C., Ferro J. A., Reinach F. C. 62 other authors 2002; Comparison of the genomes of two Xanthomonas pathogens with differing host specificities. Nature 417:459–463 [CrossRef]
     [Google Scholar]
  15. Davies J. 1994; Inactivation of antibiotics and the dissemination of resistance genes. Science 264:375–382 [CrossRef]
     [Google Scholar]
  16. Davison J. 1999; Genetic exchange between bacteria in the environment. Plasmid 42:73–91 [CrossRef]
     [Google Scholar]
  17. Del Sorbo G., Schoonbeek H., De Waard M. A. 2000; Fungal transporters involved in efflux of natural toxic compounds and fungicides. Fungal Genet Biol 30:1–15 [CrossRef]
     [Google Scholar]
  18. Dröge M., Pühler 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]
  19. Ferreira L. P., Lemos E. G., Lemos M. V. 2002; Transposon Tn1721 distribution among strains of Xylella fastidiosa. FEMS Microbiol Lett 208:163–168 [CrossRef]
     [Google Scholar]
  20. Fleißner A., Sopalla C., Weltring K. M. 2002; An ATP-binding cassette multidrug-resistance transporter is necessary for tolerance of Gibberella pulicaris to phytoalexins and virulence on potato tubers. Mol Plant–Microbe Interact 15:102–108 [CrossRef]
     [Google Scholar]
  21. Gardner M. N., Deane S. M., Rawlings D. E. 2001; Isolation of a new broad-host-range IncQ-like plasmid, pTC-F14, from the acidophilic bacterium Acidithiobacillus caldus and analysis of the plasmid replicon. J Bacteriol 183:3303–3309 [CrossRef]
     [Google Scholar]
  22. Gaynor M., Mankin A. S. 2003; Macrolide antibiotics: binding site, mechanism of action, resistance. Curr Top Med Chem 3:949–961 [CrossRef]
     [Google Scholar]
  23. Götz A., Pukall R., Smit E., Tietze E., Prager R., van Elsas J. D., Smalla K, Tschäpe H. 1996; Detection and characterization of broad-host-range plasmids in environmental bacteria by PCR. Appl Environ Microbiol 62:2621–2628
     [Google Scholar]
  24. Grant S. G., Jessee J., Bloom F. R., Hanahan D. 1990; Differential plasmid rescue from transgenic mouse DNAs into Escherichia coli methylation-restriction mutants. Proc Natl Acad Sci U S A 87:4645–4649 [CrossRef]
     [Google Scholar]
  25. Hall R. M., Collis C. M. 1995; Mobile gene cassettes and integrons: capture and spread of genes by site-specific recombination. Mol Microbiol 15:593–600
     [Google Scholar]
  26. Haneda T., Okada N., Nakazawa N., Kawakami T., Danbara H. 2001; Complete DNA sequence and comparative analysis of the 50-kilobase virulence plasmid of Salmonella enterica serovar Choleraesuis. Infect Immun 69:2612–2620 [CrossRef]
     [Google Scholar]
  27. Herdendorf T. J., McCaslin D. R., Forest K. T. 2002; Aquifex aeolicus PilT, homologue of a surface motility protein, is a thermostable oligomeric NTPase. J Bacteriol 184:6465–6471 [CrossRef]
     [Google Scholar]
  28. Higgins C. F. 2001; ABC transporters: physiology, structure and mechanism – an overview. Res Microbiol 152:205–210 [CrossRef]
     [Google Scholar]
  29. Hynes M. F., Simon R., Pühler A. 1985; The development of plasmid-free strains of Agrobacterium tumefaciens by using incompatibility with a Rhizobium meliloti plasmid to eliminate pAtC58. Plasmid 13:99–105 [CrossRef]
     [Google Scholar]
  30. Klockgether J., Reva O., Larbig K., Tummler B. 2004; Sequence analysis of the mobile genome island pKLC102 of Pseudomonas aeruginosa C. J Bacteriol 186:518–534 [CrossRef]
     [Google Scholar]
  31. Koski P., Saarilahti H., Sukupolvi S., Taira S., Riikonen P., Hurme R., Rhen M, Österlund K. 1992; A new α-helical coiled coil protein encoded by the Salmonella typhimurium virulence plasmid. J Biol Chem 267:12258–12265
     [Google Scholar]
  32. Kurtz S., Choudhuri J. V., Ohlebusch E., Schleiermacher C., Stoye J., Giegerich R. 2001; REPuter: the manifold applications of repeat analysis on a genomic scale. Nucleic Acids Res 29:4633–4642 [CrossRef]
     [Google Scholar]
  33. Kwong S. M., Yeo C. C., Chuah D., Poh C. L. 1998; Sequence analysis of plasmid pRA2 from Pseudomonas alcaligenes NCIB 9867 (P25X) reveals a novel replication region. FEMS Microbiol Lett 158:159–165 [CrossRef]
     [Google Scholar]
  34. Kwong S. M., Yeo C. C., Suwanto A., Poh C. L. 2000; Characterization of the endogenous plasmid from Pseudomonas alcaligenes NCIB 9867: DNA sequence and mechanism of transfer. J Bacteriol 182:81–90 [CrossRef]
     [Google Scholar]
  35. L'Abée-Lund T. M., Sørum H. 2002; A global non-conjugative Tet C plasmid, pRAS3, from Aeromonas salmonicida . Plasmid 47:172–181 [CrossRef]
     [Google Scholar]
  36. Lèvesque C., Piche L., Larose C., Roy P. H. 1995; PCR mapping of integrons reveals several novel combinations of resistance genes. Antimicrob Agents Chemother 39:185–191 [CrossRef]
     [Google Scholar]
  37. Liebl W., Kloos W. E., Ludwig W. 2002; Plasmid-borne macrolide resistance in Micrococcus luteus. Microbiology 148:2479–2487
     [Google Scholar]
  38. Lin C. F., Chung T. C. 1999; Cloning of erythromycin-resistance determinants and replication origins from indigenous plasmids of Lactobacillus reuteri for potential use in construction of cloning vectors. Plasmid 42:31–41 [CrossRef]
     [Google Scholar]
  39. Llanes C., Gabant P., Couturier M., Bayer L., Plesiat P. 1996; Molecular analysis of the replication elements of the broad-host-range RepA/C replicon. Plasmid 36:26–35 [CrossRef]
     [Google Scholar]
  40. Ma D., Alberti M., Lynch C., Nikaido H., Hearst J. E. 1996; The local repressor AcrR plays a modulating role in the regulation of acrAB genes of Escherichia coli by global stress signals. Mol Microbiol 19:101–112 [CrossRef]
     [Google Scholar]
  41. Mach P. A., Grimes D. J. 1982; R-plasmid transfer in a wastewater treatment plant. Appl Environ Microbiol 44:1395–1403
     [Google Scholar]
  42. Matsuoka M., Endou K., Kobayashi H., Inoue M., Nakajima Y. 1998; A plasmid that encodes three genes for resistance to macrolide antibiotics in Staphylococcus aureus. FEMS Microbiol Lett 167:221–227 [CrossRef]
     [Google Scholar]
  43. Mazel D., Davies J. 1999; Antibiotic resistance in microbes. Cell Mol Life Sci 56:742–754 [CrossRef]
     [Google Scholar]
  44. McManus P. S., Stockwell V. O., Sundin G. W., Jones A. L. 2002; Antibiotic use in plant agriculture. Annu Rev Phytopathol 40:443–465 [CrossRef]
     [Google Scholar]
  45. Meyer F., Goesmann A., McHardy A. C. & 8 other authors; 2003; GenDB–an open source genome annotation system for prokaryote genomes. Nucleic Acids Res 31:2187–2195 [CrossRef]
     [Google Scholar]
  46. Nikaido H., Zgurskaya H. I. 2001; AcrAB and related multidrug efflux pumps of Escherichia coli . J Mol Microbiol Biotechnol 3:215–218
     [Google Scholar]
  47. Noguchi N., Emura A., Matsuyama H., O'Hara K., Sasatsu M., Kono M. 1995; Nucleotide sequence and characterization of erythromycin resistance determinant that encodes macrolide 2′-phosphotransferase I in Escherichia coli . Antimicrob Agents Chemother 39:2359–2363 [CrossRef]
     [Google Scholar]
  48. Noguchi N., Takada K., Katayama J., Emura A., Sasatsu M. 2000; Regulation of transcription of the mph(A) gene for macrolide 2′-phosphotransferase I in Escherichia coli: characterization of the regulatory gene mphR(A). J Bacteriol 182:5052–5058 [CrossRef]
     [Google Scholar]
  49. Ohlsen K., Ternes T., Werner G., Wallner U., Loffler D., Ziebuhr W., Witte W., Hacker J. 2003; Impact of antibiotics on conjugational resistance gene transfer in Staphylococcus aureus in sewage. Environ Microbiol 5:711–716 [CrossRef]
     [Google Scholar]
  50. Pansegrau W., Lanka E., Barth P. T. & 7 other authors; 1994; Complete nucleotide sequence of Birmingham IncPα plasmids. Compilation and comparative analysis. J Mol Biol 239:623–663 [CrossRef]
     [Google Scholar]
  51. Partridge S. R., Brown H. J., Stokes H. W., Hall R. M. 2001; Transposons Tn1696 and Tn21 and their integrons In4 and In2 have independent origins. Antimicrob Agents Chemother 45:1263–1270 [CrossRef]
     [Google Scholar]
  52. Paulsen I. T., Park J. H., Choi P. S., Saier M. H. Jr 1997; A family of Gram-negative bacterial outer membrane factors that function in the export of proteins, carbohydrates, drugs and heavy metals from Gram-negative bacteria. FEMS Microbiol Lett 156:1–8 [CrossRef]
     [Google Scholar]
  53. Rawlings D. E., Tietze E. 2001; Comparative biology of IncQ and IncQ-like plasmids. Microbiol Mol Biol Rev 65:481–496 [CrossRef]
     [Google Scholar]
  54. Rhodes G., Huys G., Swings J., McGann P., Hiney M., Smith P., Pickup R. W. 2000; Distribution of oxytetracycline resistance plasmids between aeromonads in hospital and aquaculture environments: implication of Tn1721 in dissemination of the tetracycline resistance determinanttetA . Appl Environ Microbiol 66:3883–3890 [CrossRef]
     [Google Scholar]
  55. Roberts R. C., Helinski D. R. 1992; Definition of a minimal plasmid stabilization system from the broad-host-range plasmid RK2. J Bacteriol 174:8119–8132
     [Google Scholar]
  56. Roberts M. C., Sutcliffe J., Courvalin P., Jensen L. B., Rood J., Seppala H. 1999; Nomenclature for macrolide and macrolide-lincosamide-streptogramin B resistance determinants. Antimicrob Agents Chemother 43:2823–2830
     [Google Scholar]
  57. Rohrer J., Rawlings D. E. 1992; Sequence analysis and characterization of the mobilization region of a broad-host-range plasmid, pTF-FC2, isolated from Thiobacillus ferrooxidans . J Bacteriol 174:6230–6237
     [Google Scholar]
  58. Rowe-Magnus D. A., Mazel D. 1999; Resistance gene capture. Curr Opin Microbiol 2:483–488 [CrossRef]
     [Google Scholar]
  59. Saier M. H. Jr, Paulsen I. T. 2001; Phylogeny of multidrug transporters. Semin Cell Dev Biol 12:205–213 [CrossRef]
     [Google Scholar]
  60. Sakai D., Komano T. 2002; Genes required for plasmid R64 thin-pilus biogenesis: identification and localization of products of the pilK, pilM, pilO, pilP, pilR, and pilT genes. J Bacteriol 184:444–451 [CrossRef]
     [Google Scholar]
  61. Sambrook J., Fritsch E. F., Maniatis T. 1989 Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
     [Google Scholar]
  62. Schäfer A., Tauch A., Kalinowski J., Thierbach G, Jäger W., Pühler A. 1994; Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome ofCorynebacterium glutamicum . Gene 145:69–73 [CrossRef]
     [Google Scholar]
  63. Schlüter A., Heuer H., Szczepanowski R., Forney L. J., Thomas C. M., Top E. M, Pühler A. 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]
  64. Schnabel E. L., Jones A. L. 1999; Distribution of tetracycline resistance genes and transposons among phylloplane bacteria in Michigan apple orchards. Appl Environ Microbiol 65:4898–4907
     [Google Scholar]
  65. Schneider E., Hunke S. 1998; ATP-binding-cassette (ABC) transport systems: functional and structural aspects of the ATP-hydrolyzing subunits/domains. FEMS Microbiol Rev 22:1–20 [CrossRef]
     [Google Scholar]
  66. Schoonbeek H., Del Sorbo G., De Waard M. A. 2001; The ABC transporter BcatrB affects the sensitivity of Botrytis cinerea to the phytoalexin resveratrol and the fungicide fenpiclonil. Mol Plant–Microbe Interact 14:562–571 [CrossRef]
     [Google Scholar]
  67. Sesma A., Sundin G. W., Murillo J. 1998; Closely related plasmid replicons coexisting in the phytopathogen Pseudomonas syringae show a mosaic organization of the replication region and altered incompatibility behavior. Appl Environ Microbiol 64:3948–3953
     [Google Scholar]
  68. Sesma A., Sundin G. W., Murillo J. 2000; Phylogeny of the replication regions of pPT23A-like plasmids from Pseudomonas syringae. Microbiology 146:2375–2384
     [Google Scholar]
  69. Sèveno N. A., Kallifidas D., Smalla K., van Elsas J. D., Collard J. M., Karagouni A. D., Wellington E. M. H. 2002; Occurrence and reservoirs of antibiotic resistance genes in the environment. Reviews Med Microbiol 13:15–27 [CrossRef]
     [Google Scholar]
  70. Silva J., Aguilar C., Ayala G., Estrada M. A., Garza-Ramos U., Lara-Lemus R., Ledezma L. 2000; TLA-1: a new plasmid-mediated extended-spectrum β-lactamase from Escherichia coli . Antimicrob Agents Chemother 44:997–1003 [CrossRef]
     [Google Scholar]
  71. Smalla K., Sobecky P. A. 2002; The prevalence and diversity of mobile genetic elements in bacterial communities of different environmental habitats: insights gained from different methodological approaches. FEMS Microbiol Ecol 42:165–175 [CrossRef]
     [Google Scholar]
  72. Staden R. 1996; The Staden sequence analysis package. Mol Biotechnol 5:233–241 [CrossRef]
     [Google Scholar]
  73. Stratton C. W. 1998; Macrolides, lincosamides, and streptogramins: new agents and new roles. Antimicrob Infect Dis Newsl 17:89–92 [CrossRef]
     [Google Scholar]
  74. Sundin G. W. 2002; Distinct recent lineages of the strA-strB streptomycin-resistance genes in clinical and environmental bacteria. Curr Microbiol 45:63–69 [CrossRef]
     [Google Scholar]
  75. Sundin G. W., Bender C. L. 1996; Dissemination of the strA-strB streptomycin-resistance genes among commensal and pathogenic bacteria from humans, animals, and plants. Mol Ecol 5:133–143 [CrossRef]
     [Google Scholar]
  76. Sutcliffe J., Grebe T., Tait-Kamradt A., Wondrack L. 1996; Detection of erythromycin-resistant determinants by PCR. Antimicrob Agents Chemother 40:2562–2566
     [Google Scholar]
  77. Tatusov R. L., Natale D. A., Garkavtsev I. V. 7 other authors 2001; The COG database: new developments in phylogenetic classification of proteins from complete genomes. Nucleic Acids Res 29:22–28 [CrossRef]
     [Google Scholar]
  78. Tauch A., Bischoff N., Goesmann A., Meyer F, Schlüter A., Pühler A. 2003; The 79,370-bp conjugative plasmid pB4 consists of an IncP-1β backbone loaded with a chromate resistance transposon, the strA-strB streptomycin resistance gene pair, the oxacillinase gene blaNPS-1, and a tripartite antibiotic efflux system of the resistance-nodulation-division family. Mol Genet Genomics 268:570–584
     [Google Scholar]
  79. Tennstedt T., Szczepanowski R., Braun S., Pühler A., Schlüter A. 2003; Occurrence of integron-associated resistance gene cassettes located on antibiotic resistance plasmids isolated from a wastewater treatment plant. FEMS Microbiol Ecol 45:239–252 [CrossRef]
     [Google Scholar]
  80. Theriault G., Roy P. H., Howard K. A., Benner J. S., Brooks J. E., Waters A. F., Gingeras T. R. 1985; Nucleotide sequence of the PaeR7 restriction/modification system and partial characterization of its protein products. Nucleic Acids Res 13:8441–8461 [CrossRef]
     [Google Scholar]
  81. Tschäpe H. 1994; The spread of plasmids as a function of bacterial adaptability. FEMS Microbiol Ecol 15:23–31 [CrossRef]
     [Google Scholar]
  82. Vaisvila R., Vilkaitis G., Janulaitis A. 1995; Identification of a gene encoding a DNA invertase-like enzyme adjacent to the PaeR7I restriction-modification system. Gene 157:81–84 [CrossRef]
     [Google Scholar]
  83. van Veen H. W., Konings W. N. 1998; The ABC family of multidrug transporters in microorganisms. Biochim Biophys Acta 1365:31–36 [CrossRef]
     [Google Scholar]
  84. Vaughn J. L., Feher V. A., Bracken C., Cavanagh J. 2001; The DNA-binding domain in the Bacillus subtilis transition-state regulator AbrB employs significant motion for promiscuous DNA recognition. J Mol Biol 305:429–439 [CrossRef]
     [Google Scholar]
  85. Vester B., Douthwaite S. 2001; Macrolide resistance conferred by base substitutions in 23S rRNA. Antimicrob Agents Chemother 45:1–12 [CrossRef]
     [Google Scholar]
  86. Vivian A., Murillo J., Jackson R. W. 2001; The roles of plasmids in phytopathogenic bacteria: mobile arsenals?. Microbiology 147:763–780
     [Google Scholar]
  87. Yanisch-Perron C., Vieira J., Messing J. 1985; Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33:103–119 [CrossRef]
     [Google Scholar]
  88. Zgurskaya H. I. 2002; Molecular analysis of efflux pump-based antibiotic resistance. Int J Med Microbiol 292:95–105 [CrossRef]
     [Google Scholar]
  89. Zhanel G. G., Dueck M., Hoban D. J., Vercaigne L. M., Embil J. M., Gin A. S., Karlowsky J. A. 2001; Review of macrolides and ketolides: focus on respiratory tract infections. Drugs 61:443–498 [CrossRef]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.27317-0
Loading
Antibiotic multiresistance plasmid pRSB101 isolated from a wastewater treatment plant is related to plasmids residing in phytopathogenic bacteria and carries eight different resistance determinants including a multidrug transport system
Microbiology 150, 3613 (2004); https://doi.org/10.1099/mic.0.27317-0
/content/journal/micro/10.1099/mic.0.27317-0
/content/journal/micro/10.1099/mic.0.27317-0
Loading

Data & Media loading...

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