The complete genome sequences of four new IncN plasmids from wastewater treatment plant effluent provide new insights into IncN plasmid diversity and evolution

Plasmid

Volumn 68, Issue 1, 2012, Pages 13-24

  Eikmeyer, Felix ^a   Hadiati, Atika ^a   Szczepanowski, Rafael ^a   Wibberg, Daniel ^a   Schneiker Bekel, Susanne ^a   Rogers, Linda M ^b   Brown, Celeste J ^b   Top, Eva M ^b   Pühler, Alfred ^a   Schlüter, Andreas ^a  

^a BIELEFELD UNIVERSITY   (Germany)

^b UNIVERSITY OF IDAHO   (United States)

Author keywords

Antibiotic resistance; Conjugative transfer; Host range; IncN plasmid; Mobile genetic elements; Wastewater treatment plant

Indexed keywords

AMPICILLIN; SPECTINOMYCIN; STREPTOMYCIN; SULFONAMIDE; TETRACYCLINE; TRIMETHOPRIM;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL STRAIN; BACTERIUM IDENTIFICATION; CONTROLLED STUDY; ESCHERICHIA COLI; GENE IDENTIFICATION; GENE INSERTION SEQUENCE; GENE REPLICATION; GENE SEQUENCE; GENETIC DATABASE; GENETIC VARIABILITY; MOLECULAR EVOLUTION; MULTIDRUG RESISTANCE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PLASMID; SEWAGE EFFLUENT; WASTE WATER TREATMENT PLANT;

BASE SEQUENCE; CONSERVED SEQUENCE; DNA REPLICATION; DNA TRANSPOSABLE ELEMENTS; DRUG RESISTANCE, MICROBIAL; DRUG RESISTANCE, MULTIPLE, BACTERIAL; ESCHERICHIA COLI; GENE TRANSFER, HORIZONTAL; INTEGRONS; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLASMIDS; REPLICATION ORIGIN; WASTE DISPOSAL, FLUID;

ENTEROBACTERIACEAE; ESCHERICHIA COLI;

EID: 84861750651     PISSN: 0147619X     EISSN: 10959890     Source Type: Journal    
DOI: 10.1016/j.plasmid.2012.01.011     Document Type: Article

References (89)

1. Akiyama T., Savin M.C. Populations of antibiotic-resistant coliform bacteria change rapidly in a wastewater effluent dominated stream. Sci. Total Environ. 2010, 408(24):6192-6201.
2. Akiyama T., Asfahl K.L., Savin M.C. Broad-host-range plasmids in treated wastewater effluent and receiving streams. J. Environ. Qual. 2010, 39(6):2211-2215.
3. Allmeier H., Cresnar B., Greck M., Schmitt R. Complete nucleotide sequence of Tn1721: gene organization and a novel gene product with features of a chemotaxis protein. Gene 1992, 111(1):11-20.
4. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 1990, 215(3):403-410.
5. Auerbach E.A., Seyfried E.E., McMahon K.D. Tetracycline resistance genes in activated sludge wastewater treatment plants. Water Res. 2007, 41(5):1143-1151.
6. Belogurov A.A., Delver E.P., Rodzevich O.V. Plasmid pKM101 encodes two nonhomologous antirestriction proteins (ArdA and ArdB) whose expression is controlled by homologous regulatory sequences. J. Bacteriol. 1993, 175(15):4843-4850.
7. Bortolaia V., Guardabassi L., Trevisani M., Bisgaard M., Venturi L., Bojesen A.M. High diversity of extended-spectrum β-lactamases in Escherichia coli isolates from Italian broiler flocks. Antimicrob. Agents Chemother. 2010, 54(4):1623-1626.
8. Bundesamt für Verbraucherschutz und Lebensmittelsicherheit, 2008. Germap 2008: Bericht über den Antibiotikaverbrauch und die Verbreitung von Antibiotikaresistenzen in der Human- und Veterinärmedizin in Deutschland, 1. Aufl. ed. Antiinfectives Intelligence, Rheinbach.
9. Carattoli A. Resistance plasmid families in Enterobacteriaceae. Antimicrob. Agents Chemother. 2009, 53(6):2227-2238.
10. Carattoli A., Aschbacher R., March A., Larcher C., Livermore D.M., Woodford N. Complete nucleotide sequence of the IncN plasmid pKOX105 encoding VIM-1, QnrS1 and SHV-12 proteins in Enterobacteriaceae from Bolzano, Italy compared with IncN plasmids encoding KPC enzymes in the USA. J. Antimicrob. Chemother. 2010, 65(10):2070-2075.
11. Chiou C.S., Jones A.L. Nucleotide sequence analysis of a transposon (Tn5393) carrying streptomycin resistance genes in Erwinia amylovora and other gram-negative bacteria. J. Bacteriol. 1993, 175(3):732-740.
12. Christie P.J. Bacterial type IV secretion: conjugation systems adapted to deliver effector molecules to host cells. Trends Microbiol. 2000, 8(8):354.
13. Clerch B., Bravo J.M., Llagostera M. Efficiency of MucAB and Escherichia coli UmuDC proteins in quinolone and UV mutagenesis in Salmonella typhimurium: effect of MucA and UmuD processing. Mutat. Res. 1996, 349(2):201-208.
14. Performance Standards for Antimicrobial Susceptibility Testing: Twentieth Informational Supplement M100-S20 2010, Clinical and Laboratory Standards Institute, Clinical and Laboratory Standards Institute, Wayne, PA.
15. CTX-M genes in different plasmids from German clinical Escherichia coli isolates. J. Med. Microbiol. 2010, 59(Pt 5):580-587.
16. de Gelder L., Ponciano J.M., Joyce P., Top E.M. Stability of a promiscuous plasmid in different hosts: no guarantee for a long-term relationship. Microbiology 2007, 153(2):452-463.
17. Delver E.P., Belogurov A.A. Organization of the leading region of IncN plasmid pKM101 (R46): a regulation controlled by CUP sequence elements. J. Mol. Biol. 1997, 271(1):13-30.
18. ESBL and surrounding genes in Spanish clinical isolates of Escherichia coli and Klebsiella pneumoniae. J. Antimicrob. Chemother. 2009, 63(1):60-66.
19. Dröge M., Pühler A., Selbitschka W. Phenotypic and molecular characterization of conjugative antibiotic resistance plasmids isolated from bacterial communities of activated sludge. Mol. Gen. Genet. 2000, 263(3):471-482.
20. Drønen A.K., Torsvik V., Goksøyr J., Top E.M. Effect of mercury addition on plasmid incidence and gene mobilizing capacity in bulk soil. FEMS Microbiol. Ecol. 1998, 27(4):381-394.
21. Foster T.J., Davis M.A., Roberts D.E., Takeshita K., Kleckner N. Genetic organization of transposon Tn10. Cell 1981, 23(1):201-213.
22. Frost L.S., Leplae R., Summers A.O., Toussaint A. Mobile genetic elements: the agents of open source evolution. Nat. Rev. Microbiol. 2005, 3(9):722-732.
23. Garcillán-Barcia M.P., Francia M.V., de La Cruz F. The diversity of conjugative relaxases and its application in plasmid classification. FEMS Microbiol. Rev. 2009, 33(3):657-687.
24. González-Zorn B., Catalan A., Escudero J.A., Domínguez L., Teshager T., Porrero C., Moreno M.A. Genetic basis for dissemination of armA. J. Antimicrob. Chemother. 2005, 56(3):583-585.
25. KPC carbapenemase genes on plasmids from Klebsiella strains isolated in a New York City hospital. Antimicrob. Agents Chemother. 2009, 53(5):1998-2004.
26. Götz A., Pukall R., Smit E., Tietze E., Prager R., Tschäpe H., van Elsas J.D., Smalla K. Detection and characterization of broad-host-range plasmids in environmental bacteria by PCR. Appl. Environ. Microbiol. 1996, 62(7):2621-2628.
27. Grant S.G., Jessee J., Bloom F.R., Hanahan D. Differential plasmid rescue from transgenic mouse DNAs into Escherichia coli methylation-restriction mutants. Proc. Natl Acad. Sci. USA 1990, 87(12):4645-4649.
28. Halling S.M., Simons R.W., Way J.C., Walsh R.B., Kleckner N. DNA sequence organization of IS10-right of Tn10 and comparison with IS10-left. Proc. Natl Acad. Sci. USA 1982, 79(8):2608-2612.
29. Hengen P.N., Denicourt D., Iyer V.N. Isolation and characterization of kikA, a region on IncN group plasmids that determines killing of Klebsiella oxytoca. J. Bacteriol. 1992, 174(9):3070-3077.
30. Heuer H., Szczepanowski R., Schneiker S., Pühler A., Top E.M., Schlüter A. The complete sequences of plasmids pB2 and pB3 provide evidence for a recent ancestor of the IncP-1β group without any accessory genes. Microbiology 2004, 150(Pt 11):3591-3599.
31. Holcík M., Iyer V.N. Structure and mode of action of kikA, a genetic region lethal to Klebsiella oxytoca and associated with conjugative antibiotic-resistance plasmids of the IncN group. Plasmid 1996, 35(3):189-203.
32. Holcík M., Rodríguez M., Couse A., Cherton-Horvat G., Iyer V.N. Conditionally lethal genes in the N pilus region of plasmid pCU1. Plasmid 1999, 42(1):53-59.
33. Hölzel C.S., Schwaiger K., Harms K., Küchenhoff H., Kunz A., Meyer K., Müller C., Bauer J. Sewage sludge and liquid pig manure as possible sources of antibiotic resistant bacteria. Environ. Res. 2010, 110(4):318-326.
34. Hynes M.F., Simon R., Pühler A. The development of plasmid-free strains of Agrobacterium tumefaciens by using incompatibility with a Rhizobium meliloti plasmid to eliminate pAtC58. Plasmid 1985, 13(2):99-105.
35. Johnson T.J., Wannemuehler Y.M., Johnson S.J., Logue C.M., White D.G., Doetkott C., Nolan L.K. Plasmid replicon typing of commensal and pathogenic Escherichia coli isolates. Appl. Environ. Microbiol. 2007, 73(6):1976-1983.
36. Krishnan B.R., Iyer V.N. Host ranges of the IncN group plasmid pCU1 and its minireplicon in gram-negative purple bacteria. Appl. Environ. Microbiol. 1988, 54(9):2273-2276.
37. Krishnan B.R., Iyer V.N. IncN plasmid replicon. A deletion and subcloning analysis. J. Mol. Biol. 1990, 213(4):777-788.
38. Kulakauskas S., Lubys A., Ehrlich S.D. DNA restriction-modification systems mediate plasmid maintenance. J. Bacteriol. 1995, 177(12):3451-3454.
39. Kumar S., Nei M., Dudley J., Tamura K. MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief. Bioinform. 2008, 9(4):299-306.
40. Kumarasamy K.K., Toleman M.A., Walsh T.R., Bagaria J., Butt F., Balakrishnan R., Chaudhary U., Doumith M., Giske C.G., Irfan S., Krishnan P., Kumar A.V., Maharjan S., Mushtaq S., Noorie T., Paterson D.L., Pearson A., Perry C., Pike R., Rao B., Ray U., Sarma J.B., Sharma M., Sheridan E., Thirunarayan M.A., Turton J., Upadhyay S., Warner M., Welfare W., Livermore D.M., Woodford N. Emergence of a new antibiotic resistance mechanism in India, Pakistan, and the UK: a molecular, biological, and epidemiological study. Lancet Infect. Dis. 2010, 10(9):597-602.
41. Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., Valentin F., Wallace I.M., Wilm A., Lopez R., Thompson J.D., Gibson T.J., Higgins D.G. Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23(21):2947-2948.
42. Mendiola M.V., Jubete Y., de La Cruz F. DNA sequence of IS91 and identification of the transposase gene. J. Bacteriol. 1992, 174(4):1345-1351.
43. Meyer F., Goesmann A., McHardy A.C., Bartels D., Bekel T., Clausen J., Kalinowski J., Linke B., Rupp O., Giegerich R., Pühler A. GenDB-an open source genome annotation system for prokaryote genomes. Nucleic Acids Res. 2003, 31(8):2187-2195.
44. VIM-1 metallo-beta-lactamase gene in Klebsiella pneumoniae. Antimicrob. Agents Chemother. 2010, 54(10):4497-4502.
45. CTX-M-1 between commensal Escherichia coli in pigs and farm workers. Antimicrob. Agents Chemother. 2009, 53(4):1709-1711.
46. Moré M.I., Pohlman R.F., Winans S.C. Genes encoding the pKM101 conjugal mating pore are negatively regulated by the plasmid-encoded KorA and KorB proteins. J. Bacteriol. 1996, 178(15):4392-4399.
47. Moura A., Henriques I., Smalla K., Correia A. Wastewater bacterial communities bring together broad-host range plasmids, integrons and a wide diversity of uncharacterized gene cassettes. Res. Microbiol. 2010, 161(1):58-66.
48. Norberg P., Bergstrom M., Jethava V., Dubhashi D., Hermansson M. The IncP-1 plasmid backbone adapts to different host bacterial species and evolves through homologous recombination. Nat. Commun. 2011, 2:268.
49. Norman A., Hansen L.H., Sørensen S.J. Conjugative plasmids: vessels of the communal gene pool. Philos. Trans. R. Soc. B: Biol. Sci. 2009, 364(1527):2275-2289.
50. Novais A., Cantón R., Moreira R., Peixe L., Baquero F., Coque T.M. Emergence and dissemination of Enterobacteriaceae isolates producing CTX-M-1-like enzymes in Spain are associated with IncFII (CTX-M-15) and broad-host-range (CTX-M-1, -3, and -32) plasmids. Antimicrob. Agents Chemother. 2007, 51(2):796-799.
51. Ohtsubo H., Ohtsubo E. Nucleotide sequence of an insertion element, IS1. Proc. Natl Acad. Sci. USA 1978, 75(2):615-619.
52. Ojo K.K., Kehrenberg C., Schwarz S., Odelola H.A. Identification of a complete dfrA14 gene cassette integrated at a secondary site in a resistance plasmid of uropathogenic Escherichia coli from Nigeria. Antimicrob. Agents Chemother. 2002, 46(6):2054-2055.
53. Papp P.P., Iyer V.N. Determination of the binding sites of RepA, a replication initiator protein of the basic replicon of the IncN group plasmid pCU1. J. Mol. Biol. 1995, 246(5):595-608.
54. Pasquali F. Physical linkage of Tn3 and part of Tn1721 in a tetracycline and ampicillin resistance plasmid from Salmonella Typhimurium. J. Antimicrob. Chemother. 2005, 55(4):562.
55. Paterson E.S., Moré M.I., Pillay G., Cellini C., Woodgate R., Walker G.C., Iyer V.N., Winans S.C. Genetic analysis of the mobilization and leading regions of the IncN plasmids pKM101 and pCU1. J. Bacteriol. 1999, 181(8):2572-2583.
56. Pohlman R.F., Liu F., Wang L., Moré M.I., Winans S.C. Genetic and biochemical analysis of an endonuclease encoded by the IncN plasmid pKM101. Nucleic Acids Res. 1993, 21(21):4867-4872.
57. Pohlman R.F., Genetti H.D., Winans S.C. Entry exclusion of the IncN plasmid pKM101 is mediated by a single hydrophilic protein containing a lipid attachment motif. Plasmid 1994, 31(2):158-165.
58. Poirel L., Bonnin R.A., Nordmann P. Analysis of the resistome of a multidrug-resistant NDM-1-producing Escherichia coli strain by high-throughput genome sequencing. Antimicrob. Agents Chemother. 2011, 55(9):4224-4229.
59. Rice P., Longden I., Bleasby A. EMBOSS: the European molecular biology open software suite. Trends Genet. 2000, 16(6):276-277.
60. Rodríguez M., Holcík M., Iyer V.N. Lethality and survival of Klebsiella oxytoca evoked by conjugative IncN group plasmids. J. Bacteriol. 1995, 177(22):6352-6361.
61. Rotheim M.B., Love B., Thatte V., Iyer V.N. A demonstration that pCU1 tra gene products are not required in the killing of Klebsiella pneumoniae. Plasmid 1988, 19(2):161-163.
62. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 1987, 4(4):406-425.
63. Sambrook J., Russell D.W. Molecular Cloning: A Laboratory Manual 2001, Cold Spring Harbor laboratory press, Cold Spring Harbor, NY. third ed.
64. Santini J.M., Stanisich V.A. Both the fipA gene of pKM101 and the pifC gene of F inhibit conjugal transfer of RP1 by an effect on traG. J. Bacteriol. 1998, 180(16):4093-4101.
65. Schlüter A., Heuer H., Szczepanowski R., Forney L.J., Thomas C.M., Pühler A., Top E.M. 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 2003, 149(Pt 11):3139-3153.
66. Schlüter A., Heuer H., Szczepanowski R., Poler S.M., Schneiker S., Pühler A., Top E.M. Plasmid pB8 is closely related to the prototype IncP-1β plasmid R751 but transfers poorly to Escherichia coli and carries a new transposon encoding a small multidrug resistance efflux protein. Plasmid 2005, 54(2):135-148.
67. Schlüter A., Krahn I., Kollin F., Bönemann G., Stiens M., Szczepanowski R., Schneiker S., Pühler A. IncP-1-β plasmid pGNB1 isolated from a bacterial community from a wastewater treatment plant mediates decolorization of triphenylmethane dyes. Appl. Environ. Microbiol. 2007, 73(20):6345-6350.
68. Schlüter A., Szczepanowski R., Pühler A., Top E.M. Genomics of IncP-1 antibiotic resistance plasmids isolated from wastewater treatment plants provides evidence for a widely accessible drug resistance gene pool. FEMS Microbiol. Rev. 2007, 31(4):449-477.
69. Schlüter A., Krause L., Szczepanowski R., Goesmann A., Pühler A. Genetic diversity and composition of a plasmid metagenome from a wastewater treatment plant. J. Biotechnol. 2008, 136(1-2):65-76.
70. Schneiker S., Keller M., Dröge M., Lanka E., Pühler A., Selbitschka W. The genetic organization and evolution of the broad host range mercury resistance plasmid pSB102 isolated from a microbial population residing in the rhizosphere of alfalfa. Nucleic Acids Res. 2001, 29(24):5169-5181.
71. Scholz P., Haring V., Wittmann-Liebold B., Ashman K., Bagdasarian M., Scherzinger E. Complete nucleotide sequence and gene organization of the broad-host-range plasmid RSF1010. Gene 1989, 75(2):271-288.
72. Schröder G., Lanka E. The mating pair formation system of conjugative plasmids - A versatile secretion machinery for transfer of proteins and DNA. Plasmid 2005, 54(1):1-25.
73. CTX-M-24 from Klebsiella pneumoniae. J. Antimicrob. Chemother. 2008, 62(6):1252-1256.
74. Suzuki H., Yano H., Brown C.J., Top E.M. Predicting plasmid promiscuity based on genomic signature. J. Bacteriol. 2010, 192(22):6045-6055.
75. Szczepanowski R., Krahn I., Linke B., Goesmann A., Pühler A., Schlüter A. 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 2004, 150(Pt 11):3613-3630.
76. Szczepanowski R., Krahn I., Bohn N., Pühler A., Schlüter A. Novel macrolide resistance module carried by the IncP-1β resistance plasmid pRSB111, isolated from a wastewater treatment plant. Antimicrob. Agents Chemother. 2007, 51(2):673-678.
77. Szczepanowski R., Linke B., Krahn I., Gartemann K.-H., Gützkow T., Eichler W., Pühler A., Schlüter A. Detection of 140 clinically relevant antibiotic-resistance genes in the plasmid metagenome of wastewater treatment plant bacteria showing reduced susceptibility to selected antibiotics. Microbiology 2009, 155(Pt 7):2306-2319.
78. Szczepanowski R., Eikmeyer F., Harfmann J., Blom J., Rogers L.M., Top E.M., Schlüter A. Sequencing and comparative analysis of IncP-1α antibiotic resistance plasmids reveal a highly conserved backbone and differences within accessory regions. J. Biotechnol. 2011, 155(1):95-103.
79. Szpirer C., Top E., Couturier M., Mergeay M. Retrotransfer or gene capture: a feature of conjugative plasmids, with ecological and evolutionary significance. Microbiology 1999, 145(Pt 12):3321-3329.
80. Tamura K., Nei M., Kumar S. Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc. Natl Acad. Sci. USA 2004, 101(30):11030-11035.
81. Tamura K., Dudley J., Nei M., Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) Software Version 4.0. Mol. Biol. Evol. 2007, 24(8):1596-1599.
82. Tardif G., Grant R.B. Charaterization of the host range of the N plasmids. Plasmids and transposons. Environmental effects and maintenance mechanisms; Proceedings of the 4. Annual Symposium on the Scientific Basis of Medicine held May 24-25 1979 at Dalhousie Univ. Halifax Nova Scotia 1980, 351-359. Acad. Pr., New York. C. Stuttard (Ed.).
83. Tardif G., Grant R.B. Transfer of IncN plasmids to Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 1982, 22(1):142-144.
84. NPS-1, and a tripartite antibiotic efflux system of the resistance-nodulation-division family. Mol. Gen. Genomics. 2003, 268(5):570-584.
85. Tennstedt T., Szczepanowski R., Krahn I., Pühler A., Schlüter A. Sequence of the 68,869 bp IncP-1α plasmid pTB11 from a waste-water treatment plant reveals a highly conserved backbone, a Tn402-like integron and other transposable elements. Plasmid 2005, 53(3):218-238.
86. Thatte V., Gill S., Iyer V.N. Regions on plasmid pCU1 required for the killing of Klebsiella pneumoniae. J. Bacteriol. 1985, 163(3):1296-1299.
87. Treangen T.J., Messeguer X. M-GCAT: interactively and efficiently constructing large-scale multiple genome comparison frameworks in closely related species. BMC Bioinf. 2006, 7:433.
88. Villa L., García-Fernández A., Fortini D., Carattoli A. Replicon sequence typing of IncF plasmids carrying virulence and resistance determinants. J. Antimicrob. Chemother. 2010, 65(12):2518-2529.
89. Zhao F., Hou H., Bao Q., Wu J. PGA4genomics for comparative genome assembly based on genetic algorithm optimization. Genomics 2009, 94(4):284-286.