Research Article
No access
Published Online: 1 June 2017

A Novel Plasmid, pSx1, Harboring a New Tn1696 Derivative from Extensively Drug-Resistant Shewanella xiamenensis Encoding OXA-416

Publication: Microbial Drug Resistance
Volume 23, Issue Number 4

Abstract

The whole genome sequencing of extensively drug-resistant Shewanella xiamenensis T17 isolated from hospital effluents in Algeria revealed the presence of a novel 268.4 kb plasmid designated pSx1, which carries several antibiotic-resistance genes in the novel Tn1696 derivative (Tn6297), in addition to the chromosomal blaOXA-48-like gene (blaOXA-416). The presence of the plasmid was confirmed by nuclease S1-PFGE analysis and transformation by electroporation into Escherichia coli DH10B. Tn6297 contains an In27 class 1 integron harboring the dfrA12-orfF-aadA2 array, msr(E) and mph(E) associated with IS26; a new efflux pump multidrug resistance composite transposon delimited by two ISEc29s; Tn-tet harboring tetR and tetA(C); a class 1 integron with the qacG gene cassette; qnrVC6 and dfrA23 associated with ISCR1; and a complex class 1 integron In4-like containing aacC1, aadA1, blaVEB-16, catA2, sul1Δ, cmlA9, tetR, tetA(G), aac(6′)-II, and blaPSE-1. Its mer operon carries merB, but lacks merC, in contrast to Tn1696 and Tn21. This study represents the first characterization of a multidrug-resistant transposon and multidrug resistance plasmid in Shewanella and is the first report of blaOXA-416 in Algeria, providing evidence that Shewanella spp. could be an important reservoir and vehicle for drug resistance genes.

Get full access to this article

View all available purchase options and get full access to this article.

References

1.
Normark B.H., and Normark S. 2002. Evolution and spread of antibiotic resistance. J. Intern. Med. 252:91–106.
2.
Partridge S.R. 2011. Analysis of antibiotic resistance regions in Gram-negative bacteria. FEMS Microbiol. Rev. 35:820–855.
3.
D'Costa V.M., Griffiths E., and Wright G.D. 2007. Expanding the soil antibiotic resistome: exploring environmental diversity. Curr. Opin. Microbiol. 10:481–489.
4.
Huang J., Sun B., and Zhang X. 2010. Shewanella xiamenensis sp. nov., isolated from coastal sea sediment. Int. J. Syst. Evol. Microbiol. 60:1585–1589.
5.
Zong Z. 2011. Nosocomial peripancreatic infection associated with Shewanella xiamenensis. J. Med. Microbiol. 60:1387–1390.
6.
Antonelli A., Di Palo D.M., Galano A., Becciani S., Montagnani C., Pecile P., Galli L., and Rossolini G.M. 2015. Intestinal carriage of Shewanella xiamenensis simulating carriage of OXA-48-producing Enterobacteriaceae. Diagn. Microbiol. Infect. Dis. 82:1–3.
7.
Heritier C., Poirel L., and Nordmann P. 2004. Genetic and biochemical characterization of a chromosome-encoded carbapenem-hydrolyzing ambler class D β-lactamase from Shewanella algae. Antimicrob. Agents Chemother. 48:1670–1675.
8.
Poirel L., Heritier C., and Nordmann P. 2004. Chromosome-encoded ambler class D β-lactamase of Shewanella oneidensis as a progenitor of carbapenem-hydrolyzing oxacillinase. Antimicrob. Agents Chemother. 48:348–351.
9.
Poirel L., Rodriguez-Martinez J.M., Mammeri H., Liard A., and Nordmann P. 2005. Origin of plasmid-mediated quinolone resistance determinant QnrA. Antimicrob. Agents Chemother. 49:3523–3525.
10.
Potron A., Poirel L., and Nordmann P. 2011. Origin of OXA-181, an emerging carbapenem-hydrolyzing oxacillinase, as a chromosomal gene in Shewanella xiamenensis. Antimicrob. Agents Chemother. 55:4405–4407.
11.
Zong Z. 2012. Discovery of blaOXA-199, a chromosome-based blaOXA-48-like variant, in Shewanella xiamenensis. PLoS One 7:e48280.
12.
Tacao M., Correia A., and Henriques I. 2013. Environmental Shewanella xiamenensis strains that carry blaOXA-48 or blaOXA-204 genes: additional proof for blaOXA-48-like gene origin. Antimicrob. Agents Chemother. 57:6399–6400.
13.
Clinical and Laboratory Standards Institute (CLSI). 2014. Performance Standards for Antimicrobial Susceptibility Testing. Twenty-Fourth Informational Supplement M100-S24. CLSI, Wayne, PA.
14.
Chin C.S., Alexander D.H., Marks P., Klammer A.A., Drake J., Heiner C., Clum A., Copeland A., Huddleston J., Eichler E.E., Turner S. W., and Korlach J. 2013. Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat. Methods 10:563–569.
15.
Alvarado A., Garcillan-Barcia M.P., and de la Cruz F. 2012. A degenerate primer MOB typing (DPMT) method to classify gamma-proteobacterial plasmids in clinical and environmental settings. PLoS One 7:e40438.
16.
Meier-Kolthoff J.P., Klenk H.P., and Goker M. 2014. Taxonomic use of DNA G + C content and DNA-DNA hybridization in the genomic age. Int. J. Syst. Evol. Microbiol. 64:352–356.
17.
Barton B.M., Harding G.P., and Zuccarelli A.J. 1995. A general method for detecting and sizing large plasmids. Anal. Biochem. 226:235–240.
18.
Hunter S.B., Vauterin P., Lambert-Fair M.A., Van Duyne M.S., Kubota K., Graves L., Wrigley D., Barrett T., and Ribot E. 2005. Establishment of a universal size standard strain for use with the PulseNet standardized pulsed-field gel electrophoresis protocols: converting the national databases to the new size standard. J. Clin. Microbiol. 43:1045–1050.
19.
Grape M., Motakefi A., Pavuluri S., and Kahlmeter G. 2007. Standard and real-time multiplex PCR methods for detection of trimethoprim resistance dfr genes in large collections of bacteria. Clin. Microbiol. Infect. 13:1112–1118.
20.
Seputiene V., Povilonis J., Ruzauskas M., Pavilonis A., and Suziedeliene E. 2010. Prevalence of trimethoprim resistance genes in Escherichia coli isolates of human and animal origin in Lithuania. J. Med. Microbiol. 59:315–322.
21.
Zhao J.Y., Mu X.D., Zhu Y.Q., Xi L., and Xiao Z. 2015. Identification of an integron containing the quinolone resistance gene qnrA1 in Shewanella xiamenensis. FEMS Microbiol. Lett. 362: fnv146.
22.
Post V., White P.A., and Hall R.M. 2010. Evolution of AbaR-type genomic resistance islands in multiply antibiotic-resistant Acinetobacter baumannii. J. Antimicrob. Chemother. 65:1162–1170.
23.
Naas T., Aubert D., Lambert T., and Nordmann P. 2006. Complex genetic structures with repeated elements, a sul-type class 1 integron, and the blaVEB extended-spectrum beta-lactamase gene. Antimicrob. Agents Chemother. 50:1745–1752.
24.
Zong Z., Partridge S.R., and Iredell J.R. 2009. A blaVEB-1 variant, blaVEB-6, associated with repeated elements in a complex genetic structure. Antimicrob. Agents Chemother. 53:1693–1697.
25.
Levings R.S., Djordjevic S.P., and Hall R.M. 2008. SGI2, a relative of Salmonella genomic island SGI1 with an independent origin. Antimicrob. Agents Chemother. 52:2529–2537.
26.
Harmer C.J., Moran R.A., and Hall R.M. 2014. Movement of IS26-associated antibiotic resistance genes occurs via a translocatable unit that includes a single IS26 and preferentially inserts adjacent to another IS26. MBio 5:e01801–e018014.
27.
Mollet B., Iida S., and Arber W. 1985. Gene organization and target specificity of the prokaryotic mobile genetic element IS26. Mol. Gen. Genet. 201:198–203.
28.
Liu M., Wong M.H., and Chen S. 2013. Molecular characterisation of a multidrug resistance conjugative plasmid from Vibrio parahaemolyticus. Int. J. Antimicrob. Agents 42:575–579.
29.
Villa L., and Carattoli A. 2005. Integrons and transposons on the Salmonella enterica serovar Typhimurium virulence plasmid. Antimicrob. Agents Chemother. 49:1194–1197.
30.
Griffin H.G., Foster T.J., Silver S., and Misra T.K. 1987. Cloning and DNA sequence of the mercuric- and organomercurial-resistance determinants of plasmid pDU1358. Proc. Natl. Acad. Sci. U.S.A. 84:3112–3116.
31.
Harmer C.J., and Hall R.M. 2014. pRMH760, a precursor of A/C(2) plasmids carrying blaCMY and blaNDM genes. Microb. Drug Resist. 20:416–423.
32.
Minakhina S., Kholodii G., Mindlin S., Yurieva O., and Nikiforov V. 1999. Tn5053 family transposons are res site hunters sensing plasmidal res sites occupied by cognate resolvases. Mol. Microbiol. 33:1059–1068.
33.
Padungtod P., Tribuddharat C., and Chuanchuen R. 2011. Widespread presence of dfrA12 and its association with dfrA12-aadA2 cassette in Salmonella enterica isolates from swine. Southeast Asian J. Trop. Med. Public Health 42:1471–1476.
34.
Dureja C., Mahajan S., and Raychaudhuri S. 2014. Phylogenetic distribution and prevalence of genes encoding class I integrons and CTX-M-15 extended-spectrum β-lactamases in Escherichia coli isolates from healthy humans in Chandigarh, India. PLoS One 9:e112551.
35.
Domingues S., Harms K., Fricke W.F., Johnsen P.J., da Silva G.J., and Nielsen K.M. 2012. Natural transformation facilitates transfer of transposons, integrons and gene cassettes between bacterial species. PLoS Pathog. 8:e1002837.
36.
Heuer H., Szczepanowski R., Schneiker S., Puhler A., Top E.M., and 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.
37.
He T., Shen J., Schwarz S., Wu C., and Wang Y. 2015. Characterization of a genomic island in Stenotrophomonas maltophilia that carries a novel floR gene variant. J. Antimicrob. Chemother. 70:1031–1036.
38.
Boyd D., Peters G.A., Cloeckaert A., Boumedine K.S., Chaslus-Dancla E., Imberechts H., and Mulvey M.R. 2001. Complete nucleotide sequence of a 43-kilobase genomic island associated with the multidrug resistance region of Salmonella enterica serovar Typhimurium DT104 and its identification in phage type DT120 and serovar Agona. J. Bacteriol. 183:5725–5732.
39.
Adams M.D., Goglin K., Molyneaux N., Hujer K.M., Lavender H., Jamison J.J., MacDonald I.J., Martin K.M., Russo T., Campagnari A.A., Hujer A.M., Bonomo R.A., and Gill S.R. 2008. Comparative genome sequence analysis of multidrug-resistant Acinetobacter baumannii. J. Bacteriol. 190:8053–8064.
40.
Chen C.C., Lin Y.C., Sheng W.H., Chen Y.C., Chang S.C., Hsia K.C., Liao M.H., and Li S.Y. 2011. Genome sequence of a dominant, multidrug-resistant Acinetobacter baumannii strain, TCDC-AB0715. J. Bacteriol. 193:2361–2362.
41.
Siebor E., and Neuwirth C. 2011. The new variant of Salmonella genomic island 1 (SGI1-V) from a Proteus mirabilis French clinical isolate harbours blaVEB-6 and qnrA1 in the multiple antibiotic resistance region. J. Antimicrob. Chemother. 66:2513–2520.

Information & Authors

Information

Published In

cover image Microbial Drug Resistance
Microbial Drug Resistance
Volume 23Issue Number 4June 2017
Pages: 429 - 436
PubMed: 27505638

History

Published in print: June 2017
Published online: 1 June 2017
Published ahead of print: 9 August 2016

Permissions

Request permissions for this article.

Topics

Authors

Affiliations

Khadidja Yousfi
Laboratoire d'Écologie Microbienne, FSNV, Université A/MIRA de Bejaia, Bejaia, Algérie.
Laboratoire de Santé Publique du Québec, Institut National de Santé Publique du Québec, Sainte-Anne-de-Bellevue, Canada.
Abdelaziz Touati
Laboratoire d'Écologie Microbienne, FSNV, Université A/MIRA de Bejaia, Bejaia, Algérie.
Brigitte Lefebvre
Laboratoire de Santé Publique du Québec, Institut National de Santé Publique du Québec, Sainte-Anne-de-Bellevue, Canada.
Éric Fournier
Laboratoire de Santé Publique du Québec, Institut National de Santé Publique du Québec, Sainte-Anne-de-Bellevue, Canada.
Jean-Charles Côté
Laboratoire de Santé Publique du Québec, Institut National de Santé Publique du Québec, Sainte-Anne-de-Bellevue, Canada.
Hafid Soualhine
Laboratoire de Santé Publique du Québec, Institut National de Santé Publique du Québec, Sainte-Anne-de-Bellevue, Canada.
Matthew Walker
National Microbiology Laboratory, Public Health Agency of Canada, Winnipeg, Canada.
Djamila Bougdour
Laboratoire d'Écologie Microbienne, FSNV, Université A/MIRA de Bejaia, Bejaia, Algérie.
Cécile Tremblay
Laboratoire de Santé Publique du Québec, Institut National de Santé Publique du Québec, Sainte-Anne-de-Bellevue, Canada.
Département de Microbiologie, Infectiologie et Immunologie, Université de Montréal, Montréal, Canada.
Sadjia Bekal
Laboratoire de Santé Publique du Québec, Institut National de Santé Publique du Québec, Sainte-Anne-de-Bellevue, Canada.
Département de Microbiologie, Infectiologie et Immunologie, Université de Montréal, Montréal, Canada.

Notes

Address correspondence to:Sadjia Bekal, PhDLaboratoire de Santé Publique du QuébecInstitut National de Santé Publique du QuébecSainte-Anne-de-BellevueQC H9X 3R5Canada
E-mail: [email protected]

Disclosure Statement

No competing financial interests exist.

Metrics & Citations

Metrics

Citations

Export citation

Select the format you want to export the citations of this publication.

View Options

Get Access

Access content

To read the fulltext, please use one of the options below to sign in or purchase access.

Society Access

If you are a member of a society that has access to this content please log in via your society website and then return to this publication.

Restore your content access

Enter your email address to restore your content access:

Note: This functionality works only for purchases done as a guest. If you already have an account, log in to access the content to which you are entitled.

View options

PDF/EPUB

View PDF/ePub

Full Text

View Full Text

Media

Figures

Other

Tables

Share

Share

Copy the content Link

Share on social media

Back to Top