Skip to main content
  • ASM
    • Antimicrobial Agents and Chemotherapy
    • Applied and Environmental Microbiology
    • Clinical Microbiology Reviews
    • Clinical and Vaccine Immunology
    • EcoSal Plus
    • Eukaryotic Cell
    • Infection and Immunity
    • Journal of Bacteriology
    • Journal of Clinical Microbiology
    • Journal of Microbiology & Biology Education
    • Journal of Virology
    • mBio
    • Microbiology and Molecular Biology Reviews
    • Microbiology Resource Announcements
    • Microbiology Spectrum
    • Molecular and Cellular Biology
    • mSphere
    • mSystems
  • Log in
  • My alerts
  • My Cart

Main menu

  • Home
  • Articles
    • Current Issue
    • Accepted Manuscripts
    • COVID-19 Special Collection
    • Archive
    • Minireviews
  • For Authors
    • Submit a Manuscript
    • Scope
    • Editorial Policy
    • Submission, Review, & Publication Processes
    • Organization and Format
    • Errata, Author Corrections, Retractions
    • Illustrations and Tables
    • Nomenclature
    • Abbreviations and Conventions
    • Publication Fees
    • Ethics Resources and Policies
  • About the Journal
    • About AAC
    • Editor in Chief
    • Editorial Board
    • For Reviewers
    • For the Media
    • For Librarians
    • For Advertisers
    • Alerts
    • AAC Podcast
    • RSS
    • FAQ
  • Subscribe
    • Members
    • Institutions
  • ASM
    • Antimicrobial Agents and Chemotherapy
    • Applied and Environmental Microbiology
    • Clinical Microbiology Reviews
    • Clinical and Vaccine Immunology
    • EcoSal Plus
    • Eukaryotic Cell
    • Infection and Immunity
    • Journal of Bacteriology
    • Journal of Clinical Microbiology
    • Journal of Microbiology & Biology Education
    • Journal of Virology
    • mBio
    • Microbiology and Molecular Biology Reviews
    • Microbiology Resource Announcements
    • Microbiology Spectrum
    • Molecular and Cellular Biology
    • mSphere
    • mSystems

User menu

  • Log in
  • My alerts
  • My Cart

Search

  • Advanced search
Antimicrobial Agents and Chemotherapy
publisher-logosite-logo

Advanced Search

  • Home
  • Articles
    • Current Issue
    • Accepted Manuscripts
    • COVID-19 Special Collection
    • Archive
    • Minireviews
  • For Authors
    • Submit a Manuscript
    • Scope
    • Editorial Policy
    • Submission, Review, & Publication Processes
    • Organization and Format
    • Errata, Author Corrections, Retractions
    • Illustrations and Tables
    • Nomenclature
    • Abbreviations and Conventions
    • Publication Fees
    • Ethics Resources and Policies
  • About the Journal
    • About AAC
    • Editor in Chief
    • Editorial Board
    • For Reviewers
    • For the Media
    • For Librarians
    • For Advertisers
    • Alerts
    • AAC Podcast
    • RSS
    • FAQ
  • Subscribe
    • Members
    • Institutions
Mechanisms of Resistance

A Novel Hybrid Plasmid Carrying Multiple Antimicrobial Resistance and Virulence Genes in Salmonella enterica Serovar Dublin

Chand S. Mangat, Sadjia Bekal, Rebecca J. Irwin, Michael R. Mulvey
Chand S. Mangat
aNational Microbiology Laboratory, Public Health Agency of Canada, Winnipeg, Manitoba, Canada
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Sadjia Bekal
bLaboratoire de santé publique du Québec, Saint-Anne-de-Bellevue, Quebec, Canada
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Rebecca J. Irwin
cCenter for Food-borne, Environmental and Zoonotic Infectious Diseases, Public Health Agency of Canada, Guelph, Ontario, Canada
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Michael R. Mulvey
aNational Microbiology Laboratory, Public Health Agency of Canada, Winnipeg, Manitoba, Canada
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
DOI: 10.1128/AAC.02601-16
  • Article
  • Figures & Data
  • Info & Metrics
  • PDF
Loading

ABSTRACT

Virulence plasmids and antibiotic resistance plasmids are usually maintained separately in Salmonella spp.; however, we report an instance of a hybrid plasmid (pN13-01125) in Salmonella enterica serovar Dublin. Review of the complete sequence of the 172,265-bp plasmid suggests that pN13-01125 is comprised of the previously described pSDVr and pSH696_135 plasmids and that the mechanism of hybridization likely involves IS6 (IS26) insertion sequence elements. The plasmid has a low conjugation frequency, confers resistance to six classes of antimicrobials, and contains a complete spv virulence operon.

TEXT

Salmonella enterica serovar Dublin (S. Dublin) is a bovine-adapted pathogen that can cause systemic and enteric infections in livestock (1, 2). Exposure to contaminated milk, meat, and infected animals can cause rare cases of human infections and invasive bacteremia (3, 4). Two related ∼80-kbp virulence plasmids are found in S. Dublin and are collectively referred to as pSDV, which encodes factors important for virulence (5, 6), and S. Dublin isolates are increasingly found to maintain plasmids that confer antimicrobial resistance (AMR) (7). We report a novel S. Dublin plasmid isolated from a bovine fecal sample that is a hybrid of known AMR and virulence plasmids.

In 2010, surveillance of clinical bovine samples by the Canadian Integrated Program for Antimicrobial Resistance Surveillance identified an S. Dublin stool isolate (N13-01125) from the western region of Canada with multiple-drug resistance (MDR) to six classes of antibiotics. Whole-genome sequencing of isolate N13-01125 DNA was carried out on the long-read-length Pacific Biosciences RSII platform using a single cell; 38.8-K reads yielded 519 Mb of sequence with an N50 read length of 19.6 kb. Genome assembly was carried out with SMRT analysis software using the hierarchical genome assembly protocol (HGAP) 3.0, and the draft assembly was polished using the RS_Resequencing.1 protocol (8). Plasmid pN13-01125 was resolved to 215-fold coverage and circularized using the Circlator v1.1.1 software (9) to a final length of 172,265 bp. BLAST analysis showed that pN13-01125 had high sequence identity to the S. Dublin virulence plasmid pSDVr (also called pOU1115; accession no. DQ115388 ) (10), which was likely formed as a cointegrate of pOU1114 and pOU1113 and notably replaced the tra operon for the pil operon. Additionally, pN13-01125 exhibited high sequence identity to the AMR plasmid pSH696_135 (accession no. JN983048 ) (11). By submission to the Center for Genomic Epidemiology typing web tool (www.genomicepidemiology.org ), plasmid incompatibility matches were found to both IncX1 and IncA/C2, which is consistent with the parental plasmids.

Mapping of the contribution of the parental plasmids to the pN13-01125 sequence was carried out using Double Act v2 (http://www.hpa-bioinfotools.org.uk/pise/double_actv2.html ) (12). Plasmids pSH696_135 and pSDVr contribute three alternating blocks of sequence each to pN13-01125 (Fig. 1). By querying the ISFinder web tool (http://www-is.biotoul.fr ), 11 IS6 family elements were identified (IS26-1 through IS26-10 and IS15DI). An IS26 element unique to pN13-01125 (IS26-1, IS26-2, IS26-3, IS26-4, IS26-5, IS26-8, IS26-9, IS26-10) was found at the junction between each parental sequence. Additionally, IS26-6 is found at a parental junction but was present within pSH696_135.

FIG 1
  • Open in new tab
  • Download powerpoint
FIG 1

Sequence features of the hybrid plasmid pN13-01125 (GenBank accession no. KX815983 ). Protein-coding sequences are represented by boxes along the plasmid backbone and are colored by function (see legend at top right). Outer and inner boxes are drawn 5′→3′ in the clockwise and anticlockwise directions, respectively. Backbone shading indicates the origin of each plasmid sequence, either pSDVr (magenta) (accession no. DQ115388 ) or pSH696_135 (blue) (accession no. JN983048 ). Dashed origin shading indicates sequence inversion with respect to parental plasmid. Complete insertion sequence elements are labeled, and their boundaries are indicated with square brackets. Pairs of 8-bp target site duplications are shown (innermost and outermost boxes); each pair has the same color, and a line indicates their position relative to their respective IS6 element. Gene functions are derived from manual BLAST searches, comparison with the annotated sequences of the parental plasmids, and the study review by Harmer and Hall (24).

The sequence of pN13-01125 between IS26-10 and IS26-2 (inclusive of IS26-1) is identical in structure to that of the parental plasmids, while the remainder of the plasmid contains many inversions. The sequence inversions were likely driven by intramolecular IS6 replication in a manner described by He and coworkers (13), where IS6 family replication leaves 8-bp inverted-target site duplications (TSDs). Mapping of the 8-bp regions surrounding each IS6 element revealed pairs of TSDs in the region where there were also many sequence inversions, suggesting that sequence inversion is driven by IS replication (Fig. 1). The rearrangements of plasmid structure is reminiscent of the structure of the AMR-virulence plasmid hybrid pSUO-SEVR1 recently found in S. enterica serovar Enteritidis (14).

MICs were determined by broth microdilution with the Sensititre system (Trek Diagnostic Systems Ltd., Westlake, OH, USA) using established breakpoints from the Clinical and Laboratory Standards Institute for the original isolate N13-01125 and Escherichia coli TOP10 cells transformed with pN13-01125 (15) (Table 1). The patterns of resistance between the N13-01125 isolate and the E. coli isolate carrying pN13-01125 were identical, suggesting that the plasmid was the sole determinant of antibiotic resistance. Streptomycin susceptibility was equivocal because of the intrinsic resistance of E. coli TOP10 cells to this antibiotic. Elevated MICs to streptomycin, β-lactams, gentamicin, chloramphenicol, sulfisoxazole, and tetracycline were attributed to the presence of plasmid-borne strAB, blaCMY-2/blaTEM-1, aadB, floR/cmlA, sul2, and a class A tetA, respectively. N13-01125 was susceptible to the combination of trimethoprim-sulfamethoxazole, meropenem, azithromycin, and both ciprofloxacin and nalidixic acid; no plasmid-borne resistance determinant for these antimicrobials was found. Resistance to xenobiotics and disinfectants may be preserved, as an intact mer operon similar to that found in pDU1358, qacED1, and sugE was maintained in the hybrid plasmid.

View this table:
  • View inline
  • View popup
TABLE 1

MICs of S. Dublin N13-01125 isolate and E. coli TOP10 cell harboring pN13-01125

We found pSH696_135 to be the best single model for the AMR parental origin of pN13-01125; however, two regions of this plasmid differ from pN13-01125. First, an IS1294b at 6.3 kb in pSH696_135 is not present in pN13-01125. As with pN13-01125, this element is not present in some IncA/C plasmids and has been found to promote the mobilization of the nearby blaCMY-2 (16, 17). Second, blaCMY-2 is a part of an ISEcp1-blaCMY-2-blc-sugE transposition unit previously described in some IncA/C plasmids; this region interrupts a tra operon and is responsible for a low observed conjugation frequency in plasmids in which it is found (18). In pSH696_135 and other plasmids, this region is duplicated and divergently arranged, whereas it is found in a single copy in pN13-01125. To test whether the pN13-01125 plasmid is mobile, we carried out conjugation experiments with an isolate of S. Dublin harboring pN13-01125 as the potential donor and either a ciprofloxacin-resistant S. Dublin or a sodium azide-resistant E. coli (J53) isolate as the potential recipient using a previously described protocol (10). Although we were able to produce transconjugants, the frequency was low at ∼10−8, which is consistent with the conjugation frequency of the virulence plasmid pSDVr and the observation that Salmonella virulence plasmids are normally vertically inherited (19).

A single continuous section, from 9.3 to 32.4 kbp, of the virulence plasmid pSDVr was not maintained in pN13-01125. Notably, the two-component systems ccdAB and vagCD involved in plasmid maintenance and the replication genes repAC from pSDVr were not present in pN13-01125. Despite the loss of these genes, pN13-01125 was stably maintained after three rounds of subculture in its native background and in E. coli TOP10 cells. Plasmid replication and stability were likely inherited from the other parental plasmid; with the exception of ∼12 kb of DNA, the entire pSH696_135 plasmid was present in the hybrid.

The spv virulence operon was present in pN13-01125, which was essential and sufficient to restore virulence in various plasmid-cured S. enterica serovars, including S. Dublin (20, 21). The hybrid plasmid also inherited the macrophage-inducible carbonic anhydrase mig-5 and the quorum-sensing factor srgB. The fimbriae biosynthetic cluster (faeAIH and fedH) was not present in the hybrid plasmid, but the impact of the loss of this biosynthetic cluster on S. Dublin virulence is unknown.

Previously, AMR-virulence hybrid plasmids were reported in S. enterica serovars Typhimurium, Cholerasuis, and Enteritidis (14, 22, 23); however, to our knowledge, this report is the first characterization of a hybrid plasmid in S. Dublin. Although pN13-01125 has not maintained fimbriae biosynthesis via the fae cluster, it has maintained the critical spv operon; furthermore, it contains 11 antibiotic and xenobiotic resistance modules, representing the greatest number found in a Salmonella AMR-virulence hybrid plasmid to date. Plasmid hybridization and gene loss may represent a focusing of advantageous genetic content, although the effects on pathogenesis and fitness are unknown. The emergence of a novel virulence-AMR plasmid in S. Dublin and the potential transmission to other Salmonella serovars are of serious concern.

Accession number(s).The sequence of plasmid pN13-01125 was deposited in GenBank under the accession number KX815983 .

ACKNOWLEDGMENT

We acknowledge David Boyd and Amrita Bharat for helpful suggestions on the figure and the manuscript.

FOOTNOTES

    • Received 9 December 2016.
    • Returned for modification 8 January 2017.
    • Accepted 28 February 2017.
    • Accepted manuscript posted online 20 March 2017.
  • © Crown copyright 2017.

The government of Australia, Canada, or the UK (“the Crown”) owns the copyright interests of authors who are government employees. The Crown Copyright is not transferable.

REFERENCES

  1. 1.↵
    1. Guerin MT,
    2. Martin SW,
    3. Darlington GA,
    4. Rajic A
    . 2005. A temporal study of Salmonella serovars in animals in Alberta between 1990 and 2001. Can J Vet Res69:88–99.
    OpenUrlPubMed
  2. 2.↵
    1. Nielsen LR
    . 2013. Review of pathogenesis and diagnostic methods of immediate relevance for epidemiology and control of Salmonella Dublin in cattle. Vet Microbiol162:1–9. doi:10.1016/j.vetmic.2012.08.003.
    OpenUrlCrossRef
  3. 3.↵
    1. Hoelzer K,
    2. Moreno Switt AI,
    3. Wiedmann M
    . 2011. Animal contact as a source of human non-typhoidal salmonellosis. Vet Res42:34. doi:10.1186/1297-9716-42-34.
    OpenUrlCrossRefPubMed
  4. 4.↵
    1. Crump JA,
    2. Medalla FM,
    3. Joyce KW,
    4. Krueger AL,
    5. Hoekstra RM,
    6. Whichard JM,
    7. Barzilay EJ
    ,Emerging Infections Program NARMS Working Group. 2011. Antimicrobial resistance among invasive nontyphoidal Salmonella enterica isolates in the United States: National Antimicrobial Resistance Monitoring System, 1996 to 2007. Antimicrob Agents Chemother55:1148–1154. doi:10.1128/AAC.01333-10.
    OpenUrlAbstract/FREE Full Text
  5. 5.↵
    1. Chiu CH,
    2. Lin TY,
    3. Ou JT
    . 1999. Prevalence of the virulence plasmids of nontyphoid Salmonella in the serovars isolated from humans and their association with bacteremia. Microbiol Immunol43:899–903. doi:10.1111/j.1348-0421.1999.tb01225.x.
    OpenUrlCrossRefPubMedWeb of Science
  6. 6.↵
    1. Tapia MD,
    2. Tennant SM,
    3. Bornstein K,
    4. Onwuchekwa U,
    5. Tamboura B,
    6. Maiga A,
    7. Sylla MB,
    8. Sissoko S,
    9. Kourouma N,
    10. Toure A,
    11. Malle D,
    12. Livio S,
    13. Sow SO,
    14. Levine MM
    . 2015. Invasive nontyphoidal Salmonella infections among children in Mali, 2002-2014: microbiological and epidemiologic features guide vaccine development. Clin Infect Dis 61(Suppl)4:S332–S338. doi:10.1093/cid/civ729.
    OpenUrlCrossRef
  7. 7.↵
    1. Davis MA,
    2. Hancock DD,
    3. Besser TE,
    4. Daniels JB,
    5. Baker KNK,
    6. Call DR
    . 2007. Antimicrobial resistance in Salmonella enterica serovar Dublin isolates from beef and dairy sources. Vet Microbiol119:221–230. doi:10.1016/j.vetmic.2006.08.028.
    OpenUrlCrossRefPubMedWeb of Science
  8. 8.↵
    1. Chin C-S,
    2. Alexander DH,
    3. Marks P,
    4. Klammer AA,
    5. Drake J,
    6. Heiner C,
    7. Clum A,
    8. Copeland A,
    9. Huddleston J,
    10. Eichler EE,
    11. Turner SW,
    12. Korlach J
    . 2013. Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat Methods10:563–569. doi:10.1038/nmeth.2474.
    OpenUrlCrossRefPubMedWeb of Science
  9. 9.↵
    1. Hunt M,
    2. Silva ND,
    3. Otto TD,
    4. Parkhill J,
    5. Keane JA,
    6. Harris SR
    . 2015. Circlator: automated circularization of genome assemblies using long sequencing reads. Genome Biol16:294. doi:10.1186/s13059-015-0849-0.
    OpenUrlCrossRefPubMed
  10. 10.↵
    1. Chu C,
    2. Feng Y,
    3. Chien A-C,
    4. Hu S,
    5. Chu C-H,
    6. Chiu C-H
    . 2008. Evolution of genes on the Salmonella Virulence plasmid phylogeny revealed from sequencing of the virulence plasmids of S. enterica serotype Dublin and comparative analysis. Genomics92:339–343. doi:10.1016/j.ygeno.2008.07.010.
    OpenUrlCrossRefPubMedWeb of Science
  11. 11.↵
    1. Han J,
    2. Lynne AM,
    3. David DE,
    4. Tang H,
    5. Xu J,
    6. Nayak R,
    7. Kaldhone P,
    8. Logue CM,
    9. Foley SL
    . 2012. DNA sequence analysis of plasmids from multidrug resistant Salmonella enterica serotype Heidelberg isolates. PLoS One7:e51160. doi:10.1371/journal.pone.0051160.
    OpenUrlCrossRef
  12. 12.↵
    1. Abbott JC,
    2. Aanensen DM,
    3. Bentley SD
    . 2007. WebACT: an online genome comparison suite. Methods Mol Biol395:57–74. doi:10.1007/978-1-59745-514-5_4.
    OpenUrlCrossRefPubMed
  13. 13.↵
    1. He S,
    2. Hickman AB,
    3. Varani AM,
    4. Siguier P,
    5. Chandler M,
    6. Dekker JP,
    7. Dyda F
    . 2015. Insertion sequence IS26 reorganizes plasmids in clinically isolated multidrug-resistant bacteria by replicative transposition. mBio6:e00762. doi:10.1128/mBio.00762-15.b.
    OpenUrlCrossRefPubMed
  14. 14.↵
    1. García V,
    2. García P,
    3. Rodríguez I,
    4. Rodicio R,
    5. Rodicio MR
    . 2016. The role of IS26 in evolution of a derivative of the virulence plasmid of Salmonella enterica serovar Enteritidis which confers multiple drug resistance. Infect Genet Evol45:246–249. doi:10.1016/j.meegid.2016.09.008.
    OpenUrlCrossRef
  15. 15.↵
    Clinical and Laboratory Standards Institute. 2016. Performance standards for antimicrobial susceptibility testing—26th ed. CLSI document M100-S26. Clinical and Laboratory Standards Institute,Wayne, PA.
  16. 16.↵
    1. Tagg KA,
    2. Iredell JR,
    3. Partridge SR
    . 2014. Complete sequencing of IncI1 sequence type 2 plasmid pJIE512b indicates mobilization of blaCMY-2 from an IncA/C plasmid. Antimicrob Agents Chemother58:4949–4952. doi:10.1128/AAC.02773-14.
    OpenUrlAbstract/FREE Full Text
  17. 17.↵
    1. Yassine H,
    2. Bientz L,
    3. Cros J,
    4. Goret J,
    5. Bébéar C,
    6. Quentin C,
    7. Arpin C
    . 2015. Experimental evidence for IS1294b-mediated transposition of the blaCMY-2 cephalosporinase gene in Enterobacteriaceae. J Antimicrob Chemother70:697–700. doi:10.1093/jac/dku472.
    OpenUrlCrossRefPubMed
  18. 18.↵
    1. Call DR,
    2. Singer RS,
    3. Meng D,
    4. Broschat SL,
    5. Orfe LH,
    6. Anderson JM,
    7. Herndon DR,
    8. Kappmeyer LS,
    9. Daniels JB,
    10. Besser TE
    . 2010. blaCMY-2-positive IncA/C plasmids from Escherichia coli and Salmonella enterica are a distinct component of a larger lineage of plasmids. Antimicrob Agents Chemother54:590–596. doi:10.1128/AAC.00055-09.
    OpenUrlAbstract/FREE Full Text
  19. 19.↵
    1. Feng Y,
    2. Liu J,
    3. Li Y-G,
    4. Cao F-L,
    5. Johnston RN,
    6. Zhou J,
    7. Liu G-R,
    8. Liu S-L
    . 2012. Inheritance of the Salmonella virulence plasmids: mostly vertical and rarely horizontal. Infect Genet Evol12:1058–1063. doi:10.1016/j.meegid.2012.03.004.
    OpenUrlCrossRefPubMed
  20. 20.↵
    1. Gulig PA,
    2. Danbara H,
    3. Guiney DG,
    4. Lax AJ,
    5. Norel F,
    6. Rhen M
    . 1993. Molecular analysis of spv virulence genes of the Salmonella virulence plasmids. Mol Microbiol7:825–830. doi:10.1111/j.1365-2958.1993.tb01172.x.
    OpenUrlCrossRefPubMedWeb of Science
  21. 21.↵
    1. Krause M,
    2. Roudier C,
    3. Fierer J,
    4. Harwood J,
    5. Guiney D
    . 1991. Molecular analysis of the virulence locus of the Salmonella Dublin plasmid pSDL2. Mol Microbiol5:307–316. doi:10.1111/j.1365-2958.1991.tb02111.x.
    OpenUrlCrossRefPubMed
  22. 22.↵
    1. Guerra B,
    2. Soto S,
    3. Helmuth R,
    4. Mendoza MC
    . 2002. Characterization of a self-transferable plasmid from Salmonella enterica serotype Typhimurium clinical isolates carrying two integron-borne gene cassettes together with virulence and drug resistance genes. Antimicrob Agents Chemother46:2977–2981. doi:10.1128/AAC.46.9.2977-2981.2002.
    OpenUrlAbstract/FREE Full Text
  23. 23.↵
    1. Chu C,
    2. Chiu CH,
    3. Wu WY,
    4. Chu CH,
    5. Liu TP,
    6. Ou JT
    . 2001. Large drug resistance virulence plasmids of clinical isolates of Salmonella enterica serovar Choleraesuis. Antimicrob Agents Chemother45:2299–2303. doi:10.1128/AAC.45.8.2299-2303.2001.
    OpenUrlAbstract/FREE Full Text
  24. 24.↵
    1. Harmer CJ,
    2. Hall RM
    . 2015. The A to Z of A/C plasmids. Plasmid80:63–82. doi:10.1016/j.plasmid.2015.04.003.
    OpenUrlCrossRefPubMed
PreviousNext
Back to top
Download PDF
Citation Tools
A Novel Hybrid Plasmid Carrying Multiple Antimicrobial Resistance and Virulence Genes in Salmonella enterica Serovar Dublin
Chand S. Mangat, Sadjia Bekal, Rebecca J. Irwin, Michael R. Mulvey
Antimicrobial Agents and Chemotherapy May 2017, 61 (6) e02601-16; DOI: 10.1128/AAC.02601-16

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Print

Alerts
Sign In to Email Alerts with your Email Address
Email

Thank you for sharing this Antimicrobial Agents and Chemotherapy article.

NOTE: We request your email address only to inform the recipient that it was you who recommended this article, and that it is not junk mail. We do not retain these email addresses.

Enter multiple addresses on separate lines or separate them with commas.
A Novel Hybrid Plasmid Carrying Multiple Antimicrobial Resistance and Virulence Genes in Salmonella enterica Serovar Dublin
(Your Name) has forwarded a page to you from Antimicrobial Agents and Chemotherapy
(Your Name) thought you would be interested in this article in Antimicrobial Agents and Chemotherapy.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Share
A Novel Hybrid Plasmid Carrying Multiple Antimicrobial Resistance and Virulence Genes in Salmonella enterica Serovar Dublin
Chand S. Mangat, Sadjia Bekal, Rebecca J. Irwin, Michael R. Mulvey
Antimicrobial Agents and Chemotherapy May 2017, 61 (6) e02601-16; DOI: 10.1128/AAC.02601-16
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
  • Top
  • Article
    • ABSTRACT
    • TEXT
    • ACKNOWLEDGMENT
    • FOOTNOTES
    • REFERENCES
  • Figures & Data
  • Info & Metrics
  • PDF

KEYWORDS

plasmids
Salmonella enterica
Salmonella
antimicrobial activity
plasmids
virulence

Related Articles

Cited By...

About

  • About AAC
  • Editor in Chief
  • Editorial Board
  • Policies
  • For Reviewers
  • For the Media
  • For Librarians
  • For Advertisers
  • Alerts
  • AAC Podcast
  • RSS
  • FAQ
  • Permissions
  • Journal Announcements

Authors

  • ASM Author Center
  • Submit a Manuscript
  • Article Types
  • Ethics
  • Contact Us

Follow #AACJournal

@ASMicrobiology

       

ASM Journals

ASM journals are the most prominent publications in the field, delivering up-to-date and authoritative coverage of both basic and clinical microbiology.

About ASM | Contact Us | Press Room

 

ASM is a member of

Scientific Society Publisher Alliance

 

American Society for Microbiology
1752 N St. NW
Washington, DC 20036
Phone: (202) 737-3600

Copyright © 2021 American Society for Microbiology | Privacy Policy | Website feedback

Print ISSN: 0066-4804; Online ISSN: 1098-6596