1887

Abstract

A novel multidrug-resistance plasmid, pKLH80, previously isolated from MR29-12 found in ancient permafrost, was completely sequenced and analysed. In our previous studies, we focused on the pKLH80 plasmid region containing streptomycin and tetracycline resistance genes, and their mobilization with an upstream-located IS insertion sequence (IS) element. Here, we present the complete sequence of pKLH80 and analysis of its backbone genetic structure, including previously unknown features of the plasmid’s accessory region, notably a novel variant of the β-lactamase gene . Plasmid pKLH80 was found to be a circular 14 835 bp molecule that has an overall G+C content of 40.3 mol% and encodes 20 putative ORFs. There are two distinctive functional modules within the plasmid backbone sequence: (i) the replication module consisting of and the region; and (ii) the mobilization module consisting of , and . All of the aforementioned genes share sequence identities with corresponding genes of different species of . The plasmid accessory region contains antibiotic resistance genes and IS elements (IS of the IS family, and IS and IS of the IS family) found in environmental and clinical bacterial strains of different taxa. We revealed that the sequences flanking and closely related genes from clinical bacteria are nearly identical. This fact suggests that from the environmental strain of is a progenitor of genes of clinical bacteria. We also showed that pKLH80 can replicate in different strains of and genera. The roles of IS elements in the horizontal transfer of antibiotic resistance genes are examined and discussed.

Funding
This study was supported by the:
  • Russian Foundation for Basic Research (Award 14-04-01917 and 11-04-01217)
  • Russian Academy of Sciences Presidium Program ‘Wildlife: Current State and Development’
  • Russian Academy of Sciences Presidium Program ‘Molecular and Cellular Biology’
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.079335-0
2014-10-01
2021-10-18
Loading full text...

Full text loading...

/deliver/fulltext/micro/160/10/2253.html?itemId=/content/journal/micro/10.1099/mic.0.079335-0&mimeType=html&fmt=ahah

References

  1. Actis L. A., Tolmasky M. E., Crosa J. H. ( 1999). Bacterial plasmids: replication of extrachromosomal genetic elements encoding resistance to antimicrobial compounds. Front Biosci 4:D43–D62 [View Article][PubMed]
    [Google Scholar]
  2. Altschul S. F., Madden T. L., Schäffer 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 [View Article][PubMed]
    [Google Scholar]
  3. Ambler R. P., Coulson A. F., Frère J. M., Ghuysen J. M., Joris B., Forsman M., Levesque R. C., Tiraby G., Waley S. G. ( 1991). A standard numbering scheme for the class A beta-lactamases. Biochem J 276:269–270[PubMed]
    [Google Scholar]
  4. Bennett P. M. ( 2008). Plasmid encoded antibiotic resistance: acquisition and transfer of antibiotic resistance genes in bacteria. Br J Pharmacol 153:Suppl 1S347–S357 [View Article][PubMed]
    [Google Scholar]
  5. Bonnin R. A., Poirel L., Nordmann P. ( 2012). A novel and hybrid composite transposon at the origin of acquisition of bla RTG-5 in Acinetobacter baumannii . Int J Antimicrob Agents 40:257–259 [View Article][PubMed]
    [Google Scholar]
  6. Brasch M. A., Meyer R. J. ( 1986). Genetic organization of plasmid R1162 DNA involved in conjugative mobilization. J Bacteriol 167:703–710[PubMed]
    [Google Scholar]
  7. Carattoli A. ( 2013). Plasmids and the spread of resistance. Int J Med Microbiol 303:298–304 [View Article][PubMed]
    [Google Scholar]
  8. Choury D., Aubert G., Szajnert M. F., Azibi K., Delpech M., Paul G. ( 1999). Characterization and nucleotide sequence of CARB-6, a new carbenicillin-hydrolyzing β-lactamase from Vibrio cholerae . Antimicrob Agents Chemother 43:297–301[PubMed]
    [Google Scholar]
  9. Choury D., Szajnert M. F., Joly-Guillou M. L., Azibi K., Delpech M., Paul G. ( 2000). Nucleotide sequence of the bla RTG-2 (CARB-5) gene and phylogeny of a new group of carbenicillinases. Antimicrob Agents Chemother 44:1070–1074 [View Article][PubMed]
    [Google Scholar]
  10. Cohen S. N. ( 1993). Bacterial plasmids: their extraordinary contribution to molecular genetics. Gene 135:67–76 [View Article][PubMed]
    [Google Scholar]
  11. D’Costa V. M., King C. E., Kalan L., Morar M., Sung W. W., Schwarz C., Froese D., Zazula G., Calmels F. & other authors ( 2011). Antibiotic resistance is ancient. Nature 477:457–461 [View Article][PubMed]
    [Google Scholar]
  12. Deane S. M., Rawlings D. E. ( 2004). Plasmid evolution and interaction between the plasmid addiction stability systems of two related broad-host-range IncQ-like plasmids. J Bacteriol 186:2123–2133 [View Article][PubMed]
    [Google Scholar]
  13. del Solar G., Giraldo R., Ruiz-Echevarría M. J., Espinosa M., Díaz-Orejas R. ( 1998). Replication and control of circular bacterial plasmids. Microbiol Mol Biol Rev 62:434–464[PubMed]
    [Google Scholar]
  14. Dionisio F., Conceição I. C., Marques A. C., Fernandes L., Gordo I. ( 2005). The evolution of a conjugative plasmid and its ability to increase bacterial fitness. Biol Lett 1:250–252 [View Article][PubMed]
    [Google Scholar]
  15. Dziewit L., Cegielski A., Romaniuk K., Uhrynowski W., Szych A., Niesiobedzki P., Zmuda-Baranowska M. J., Zdanowski M. K., Bartosik D. ( 2013). Plasmid diversity in arctic strains of Psychrobacter spp.. Extremophiles 17:433–444 [View Article][PubMed]
    [Google Scholar]
  16. Edgar R. C. ( 2004). muscle: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:113 [View Article][PubMed]
    [Google Scholar]
  17. Eikmeyer F., Hadiati A., Szczepanowski R., Wibberg D., Schneiker-Bekel S., Rogers L. M., Brown C. J., Top E. M., Pühler A., Schlüter A. ( 2012). The complete genome sequences of four new IncN plasmids from wastewater treatment plant effluent provide new insights into IncN plasmid diversity and evolution. Plasmid 68:13–24 [View Article][PubMed]
    [Google Scholar]
  18. Finn R. D., Mistry J., Tate J., Coggill P., Heger A., Pollington J. E., Gavin O. L., Gunasekaran P., Ceric G. & other authors ( 2010). The Pfam protein families database. Nucleic Acids Res 38:Database issueD211–D222 [View Article][PubMed]
    [Google Scholar]
  19. Garcillán-Barcia M. P., Francia M. V., de la Cruz F. ( 2009). The diversity of conjugative relaxases and its application in plasmid classification. FEMS Microbiol Rev 33:657–687 [View Article][PubMed]
    [Google Scholar]
  20. Gilichinsky D. A. ( 2002). Permafrost model of extraterrestrial habitat. Astrobiology: The Quest for the Conditions of Life125–142 Horneck G., Baumstark-Khan C. Berlin: Springer; [View Article]
    [Google Scholar]
  21. Gilichinsky D., Vishnivetskaya T., Petrova M., Spirina E., Mamykin V., Rivkina E. ( 2008). Bacteria in permafrost. Psychrophiles: From Biodiversity to Biotechnology83–102 Margesin R. Schinner F. Marx J. C. Gerday C. Berlin: Springer; [CrossRef]
    [Google Scholar]
  22. Hayes F. ( 2003). The function and organization of plasmids. Methods Mol Biol 235:1–17[PubMed]
    [Google Scholar]
  23. Heuer H., Smalla K. ( 2012). Plasmids foster diversification and adaptation of bacterial populations in soil. FEMS Microbiol Rev 36:1083–1104 [View Article][PubMed]
    [Google Scholar]
  24. Hinsa-Leasure S. M., Bhavaraju L., Rodrigues J. L., Bakermans C., Gilichinsky D. A., Tiedje J. M. ( 2010). Characterization of a bacterial community from a Northeast Siberian seacoast permafrost sample. FEMS Microbiol Ecol 74:103–113 [View Article][PubMed]
    [Google Scholar]
  25. Hong H., Ko H. J., Choi I. G., Park W. ( 2014). Previously undescribed plasmids recovered from activated sludge confer tetracycline resistance and phenotypic changes to Acinetobacter oleivorans DR1. Microb Ecol 67:369–379 [View Article][PubMed]
    [Google Scholar]
  26. Ito Y., Hirano T. ( 1997). Carbenicillin-hydrolysing penicillinase mediated by a plasmid of Proteus mirabilis and its relationship to the PSE-type enzymes of Pseudomonas aeruginosa . J Appl Microbiol 83:175–180 [View Article][PubMed]
    [Google Scholar]
  27. Joris B., Ghuysen J. M., Dive G., Renard A., Dideberg O., Charlier P., Frère J. M., Kelly J. A., Boyington J. C. & other authors ( 1988). The active-site-serine penicillin-recognizing enzymes as members of the Streptomyces R61 DD-peptidase family. Biochem J 250:313–324[PubMed]
    [Google Scholar]
  28. Kholodii G., Mindlin S., Gorlenko Z., Petrova M., Hobman J., Nikiforov V. ( 2004). Translocation of transposition-deficient (Tnd PKLH2-like) transposons in the natural environment: mechanistic insights from the study of adjacent DNA sequences. Microbiology 150:979–992 [View Article][PubMed]
    [Google Scholar]
  29. Lachapelle J., Dufresne J., Levesque R. C. ( 1991). Characterization of the bla CARB-3 gene encoding the carbenicillinase-3 β-lactamase of Pseudomonas aeruginosa . Gene 102:7–12 [View Article][PubMed]
    [Google Scholar]
  30. Lasek R., Dziewit L., Bartosik D. ( 2012). Plasmid pP62BP1 isolated from an Arctic Psychrobacter sp. strain carries two highly homologous type II restriction-modification systems and a putative organic sulfate metabolism operon. Extremophiles 16:363–376 [View Article][PubMed]
    [Google Scholar]
  31. Lukashin A. V., Borodovsky M. ( 1998). GeneMark.hmm: new solutions for gene finding. Nucleic Acids Res 26:1107–1115 [View Article][PubMed]
    [Google Scholar]
  32. Mahillon J., Chandler M. ( 1998). Insertion sequences. Microbiol Mol Biol Rev 62:725–774[PubMed]
    [Google Scholar]
  33. Mammeri H., Poirel L., Mangeney N., Nordmann P. ( 2003). Chromosomal integration of a cephalosporinase gene from Acinetobacter baumannii into Oligella urethralis as a source of acquired resistance to β-lactams. Antimicrob Agents Chemother 47:1536–1542 [View Article][PubMed]
    [Google Scholar]
  34. Marchler-Bauer A., Lu S., Anderson J. B., Chitsaz F., Derbyshire M. K., DeWeese-Scott C., Fong J. H., Geer L. Y., Geer R. C. & other authors ( 2011). CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res 39:Database issueD225–D229 [View Article][PubMed]
    [Google Scholar]
  35. Matthew M. ( 1979). Plasmid-mediated β-lactamases of Gram-negative bacteria: properties and distribution. J Antimicrob Chemother 5:349–358 [View Article][PubMed]
    [Google Scholar]
  36. Melano R., Petroni A., Garutti A., Saka H. A., Mange L., Pasterán F., Rapoport M., Rossi A., Galas M. ( 2002). New carbenicillin-hydrolyzing β-lactamase (CARB-7) from Vibrio cholerae non-O1, non-O139 strains encoded by the VCR region of the V. cholerae genome. Antimicrob Agents Chemother 46:2162–2168 [View Article][PubMed]
    [Google Scholar]
  37. Mindlin S. Z., Gorlenko Zh. M., Bass I. A., Khachikian N. A. ( 1990). [Spontaneous transformation in mixed cultures of various types of Acinetobacter and during joint growth of Acinetobacter calcoaceticus with Escherichia coli and Pseudomonas aeruginosa.]. Genetika 26:1729–1739[PubMed]
    [Google Scholar]
  38. Norberg P., Bergström M., Jethava V., Dubhashi D., Hermansson M. ( 2011). The IncP-1 plasmid backbone adapts to different host bacterial species and evolves through homologous recombination. Nat Commun 2:268 [View Article][PubMed]
    [Google Scholar]
  39. Paul G., Joly-Guillou M. L., Bergogne-Berezin E., Névot P., Philippon A. ( 1989). Novel carbenicillin-hydrolyzing β-lactamase (CARB-5) from Acinetobacter calcoaceticus var. anitratus . FEMS Microbiol Lett 50:45–50[PubMed]
    [Google Scholar]
  40. Perry J. A., Wright G. D. ( 2013). The antibiotic resistance “mobilome”: searching for the link between environment and clinic. Front Microbiol 4:138 [View Article][PubMed]
    [Google Scholar]
  41. Petrova M. A., Gorlenko Zh. M., Soina V. S., Mindlin S. Z. ( 2008). [Association of the strA–strB genes with plasmids and transposons in the present-day bacteria and in bacterial strains from permafrost]. Genetika 44:1281–1286[PubMed]
    [Google Scholar]
  42. Petrova M., Gorlenko Zh., Mindlin S. ( 2009). Molecular structure and translocation of a multiple antibiotic resistance region of a Psychrobacter psychrophilus permafrost strain. FEMS Microbiol Lett 296:190–197 [View Article][PubMed]
    [Google Scholar]
  43. Petrova M., Gorlenko Z., Mindlin S. ( 2011). Tn5045, a novel integron-containing antibiotic and chromate resistance transposon isolated from a permafrost bacterium. Res Microbiol 162:337–345 [View Article][PubMed]
    [Google Scholar]
  44. Petrova M., Shcherbatova N., Gorlenko Zh., Mindlin S. ( 2013). A new subgroup of the IS3 family and properties of its representative member ISPpy1. . Microbiology 159:1900–1910 [View Article][PubMed]
    [Google Scholar]
  45. Philippon A. M., Paul G. C., Thabaut A. P., Jacoby G. A. ( 1986). Properties of a novel carbenicillin-hydrolyzing β-lactamase (CARB-4) specified by an IncP-2 plasmid from Pseudomonas aeruginosa . Antimicrob Agents Chemother 29:519–520 [View Article][PubMed]
    [Google Scholar]
  46. Popowska M., Krawczyk-Balska A. ( 2013). Broad-host-range IncP-1 plasmids and their resistance potential. Front Microbiol 4:44 [View Article][PubMed]
    [Google Scholar]
  47. Potron A., Poirel L., Croizé J., Chanteperdrix V., Nordmann P. ( 2009). Genetic and biochemical characterization of the first extended-spectrum CARB-type β-lactamase, RTG-4, from Acinetobacter baumannii . Antimicrob Agents Chemother 53:3010–3016 [View Article][PubMed]
    [Google Scholar]
  48. Roberts R. J., Vincze T., Posfai J., Macelis D. ( 2010). REBASE – a database for DNA restriction and modification: enzymes, genes and genomes. Nucleic Acids Res 38:Database issueD234–D236 [View Article][PubMed]
    [Google Scholar]
  49. Romanenko L. A., Lysenko A. M., Rohde M., Mikhailov V. V., Stackebrandt E. ( 2004). Psychrobacter maritimus sp. nov. and Psychrobacter arenosus sp. nov., isolated from coastal sea ice and sediments of the Sea of Japan. Int J Syst Evol Microbiol 54:1741–1745 [View Article][PubMed]
    [Google Scholar]
  50. Sakurai Y., Tsukamoto K., Sawai T. ( 1991). Nucleotide sequence and characterization of a carbenicillin-hydrolyzing penicillinase gene from Proteus mirabilis . J Bacteriol 173:7038–7041[PubMed]
    [Google Scholar]
  51. Sambrook J., Russell D. W. ( 2001). Molecular Cloning: A Laboratory Manual, 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  52. Sen D., Brown C. J., Top E. M., Sullivan J. ( 2013). Inferring the evolutionary history of IncP-1 plasmids despite incongruence among backbone gene trees. Mol Biol Evol 30:154–166 [View Article][PubMed]
    [Google Scholar]
  53. Smillie C., Garcillán-Barcia M. P., Francia M. V., Rocha E. P., de la Cruz F. ( 2010). Mobility of plasmids. Microbiol Mol Biol Rev 74:434–452 [View Article][PubMed]
    [Google Scholar]
  54. Steven B., Briggs G., McKay C. P., Pollard W. H., Greer C. W., Whyte L. G. ( 2007). Characterization of the microbial diversity in a permafrost sample from the Canadian high Arctic using culture-dependent and culture-independent methods. FEMS Microbiol Ecol 59:513–523 [View Article][PubMed]
    [Google Scholar]
  55. Summers A. O. ( 2006). Genetic linkage and horizontal gene transfer, the roots of the antibiotic multi-resistance problem. Anim Biotechnol 17:125–135 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.079335-0
Loading
/content/journal/micro/10.1099/mic.0.079335-0
Loading

Data & Media loading...

Most cited this month 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