Whole-Genome Sequencing of Gentamicin-Resistant Campylobacter coli Isolated from U.S. Retail Meats Reveals Novel Plasmid-Mediated Aminoglycoside Resistance Genes

Chen, Yuansha; Mukherjee, Sampa; Hoffmann, Maria; Kotewicz, Michael L.; Young, Shenia; Abbott, Jason; Luo, Yan; Davidson, Maureen K.; Allard, Marc W.; McDermott, Patrick F.; Zhao, Shaohua

doi:10.1128/aac.00669-13

Cited by 75 publications

(56 citation statements)

References 31 publications

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“…2. In general, the novel multidrug resistance island identified in this study showed a very low similarity with the segments of pN29701 (CP004067) and SX81 (JQ655275) (16,17) but was highly similar to the segment of pCG8245 (AY701528) (14). S1 pulsed-field gel electrophoresis (S1-PFGE) and Southern hybridization verified that the aph(2Љ)-If gene was located on the chromosome instead of a plasmid (data not shown).…”

Section: Resultsmentioning

confidence: 93%

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High Prevalence and Predominance of the aph(2″)-If Gene Conferring Aminoglycoside Resistance in Campylobacter

Yao

Liu

Wang

et al. 2017

Antimicrob Agents Chemother

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Campylobacter is a major foodborne pathogen, and previous studies revealed that Campylobacter isolates from food-producing animals are increasingly resistant to gentamicin in China. The molecular epidemiology and genetic mechanisms responsible for gentamicin resistance in China have not been well understood. In this study, 607 Campylobacter isolates of chicken and swine origins collected in 2014 were analyzed, revealing that 15.6% (25/160) of the Campylobacter jejuni isolates and 79.9% (357/447) of the Campylobacter coli isolates were resistant to gentamicin. PCR detection of the gentamicin resistance genes indicated that aph(2Љ)-If was more prevalent than the previously identified aacA/aphD gene and has become the dominant gentamicin resistance determinant in Campylobacter. Transformation and wholegenome sequencing as well as long-range PCR discovered that aph(2Љ)-If was located on a chromosomal segment inserted between two conserved genes, Cj0299 and panB. Cloning of aph(2Љ)-If into gentamicin-susceptible C. jejuni NCTC 11168 confirmed its function in conferring high-level resistance to gentamicin and kanamycin. Molecular typing by pulsed-field gel electrophoresis suggested that both regional expansion of a particular clone and horizontal transmission were involved in the dissemination of the aph(2Љ)-If gene in Campylobacter. To our knowledge, this is the first report describing the high prevalence of a chromosomally encoded aph(2Љ)-If gene in Campylobacter. The high prevalence and predominance of this gene might be driven by the use of aminoglycoside antibiotics in food animal production in China and potentially compromise the usefulness of gentamicin as a therapeutic agent for Campylobacter-associated systemic infection.

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Section: Resultsmentioning

confidence: 93%

“…The aacA/aphD gene encoding a bifunctional enzyme was associated with gentamicin resistance (16). Very recently, several variants of 2Љ-phosphotransferase accounting for gentamicin resistance were identified in Campylobacter in the United States (9,17).…”

mentioning

confidence: 99%

High Prevalence and Predominance of the aph(2″)-If Gene Conferring Aminoglycoside Resistance in Campylobacter

Yao

Liu

Wang

et al. 2017

Antimicrob Agents Chemother

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“…1). Similarly to the p11601MD region encompassing tet(O) and aphA-3, the corresponding region of pN29710-1 has a higher GC content than the rest of the plasmid, suggesting acquisition from another source via horizontal gene transfer (Chen et al, 2013). These findings suggest that the tet(O)-aphA-3 cassette in p11601MD represents a minimal antimicrobial resistance locus that can become expanded in other plasmids by insertion of additional genes.…”

Section: Organization Of P11601md and Pcr-based Detection Of Homologomentioning

confidence: 83%

“…However, the accompanying ORFs (designated ORFA and ORFB) associated with a putative transposase (IS607*) upstream of aphA-3 in pCJG9 (Gibreel et al, 2004) were not detected in p11601MD. In another example, the aphA-3 of p11601MD had 100% identity to a gene annotated as 3' aminoglycoside-phosphotransferase in plasmid pN29710-1 (55,127 nt) from C. coli strain CVM N29710 (Chen et al, 2013) (Fig. 1).…”

Section: Organization Of P11601md and Pcr-based Detection Of Homologomentioning

confidence: 97%

Novel plasmid conferring kanamycin and tetracycline resistance in the turkey-derived Campylobacter jejuni strain 11601MD

Crespo

Altermann

Olson

et al. 2016

Plasmid

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In Campylobacter spp., resistance to the antimicrobials kanamycin and tetracycline is frequently associated with plasmid-borne genes. However, relatively few plasmids of Campylobacter jejuni have been fully characterized to date. A novel plasmid (p11601MD; 44,095nt) harboring tet(O) was identified in C. jejuni strain 11601MD, which was isolated from the jejunum of a turkey produced conventionally in North Carolina. Analysis of the p11601MD sequence revealed the presence of a high-GC content cassette with four genes that included tet(O) and a putative aminoglycoside transferase gene (aphA-3) highly similar to kanamycin resistance determinants. Several genes putatively involved in conjugative transfer were also identified on the plasmid. These findings will contribute to a better understanding of the distribution of potentially self-mobilizing plasmids harboring antibiotic resistance determinants in Campylobacter spp. from turkeys and other sources.

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“…It allows a single test to replace several less efficient and more expensive technologies that require specialized training. For example, it is possible to extract serotype information from a bacterial pathogen genome along with antibiotic resistance patterns and the relatedness of strains in an outbreak (2)(3)(4)(5)(6)(7)(8)(9)(10)(11)(12)(13). This will obviate the need to support multiple methodologies for the various pathogenic species.…”

Section: Outreach and Harmonization Effortsmentioning

confidence: 99%

Practical Value of Food Pathogen Traceability through Building a Whole-Genome Sequencing Network and Database

et al. 2016

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The FDA has created a United States-based open-source whole-genome sequencing network of state, federal, international, and commercial partners. The GenomeTrakr network represents a first-of-its-kind distributed genomic food shield for characterizing and tracing foodborne outbreak pathogens back to their sources. The GenomeTrakr network is leading investigations of outbreaks of foodborne illnesses and compliance actions with more accurate and rapid recalls of contaminated foods as well as more effective monitoring of preventive controls for food manufacturing environments. An expanded network would serve to provide an international rapid surveillance system for pathogen traceback, which is critical to support an effective public health response to bacterial outbreaks. R ecent devastating outbreaks associated with the consumption of fresh-cut produce have reinforced the notion that foodborne disease remains a substantial global challenge to public health. In the United States alone, one in six or an estimated 48 million people fall prey to foodborne pathogens, yielding 128,000 hospitalizations and 3,000 deaths per year (http://www.cdc.gov /foodborneburden). Economic burdens are estimated cumulatively at $152 billion dollars annually, $39 billion of which is attributed directly to the contamination of fresh, canned, and processed produce (see the Produce Safety Project, http://www .pewtrusts.org/en/about/news-room/press-releases/0001/01/01 /foodborne-illness-costs-nation-$152-billion-annually-nearly -$39-billion-loss-attributed-to-produce). Mitigating foodborne illness, at times, seems to be an intractable challenge.One longstanding problem is the ability to rapidly identify the food source of the contamination. Despite the best efforts of food safety experts, the previous technology, pulsed-field gel electrophoresis (PFGE), often lacks the resolution to effectively pinpoint the source of an outbreak. The promise of whole-genome sequencing (WGS) came in 2012 when scientists with the U.S. Food and Drug Administration's Center for Food Safety and Applied Nutrition (FDA-CFSAN) performed a retrospective outbreak study on a 2012 Salmonella outbreak that was linked to spicy tuna sushi rolls by PFGE. The clinical isolates, food isolates, and historical isolates of the same PFGE pattern were all sequenced on the Illumina MiSeq. In contrast to the PFGE results, where isolates from the current outbreak looked exactly the same as unrelated historical isolates, WGS uncovered a surprising level of resolution distinguishing all of the isolates. Moreover, the isolates from the outbreak were most closely related to a 5-year-old historical isolate that was linked to a processing facility only 8 km away from the source of the outbreak (1). This isolate was collected at the port of entry from an earlier inspection of contaminated seafood and, like many others, was saved in the freezer collection of the FDA-CFSAN. The idea that the FDA's historical isolates could all be sequenced, providing investigators with geographic clues from a ...

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Whole-Genome Sequencing of Gentamicin-Resistant Campylobacter coli Isolated from U.S. Retail Meats Reveals Novel Plasmid-Mediated Aminoglycoside Resistance Genes

Cited by 75 publications

References 31 publications

High Prevalence and Predominance of the aph(2″)-If Gene Conferring Aminoglycoside Resistance in Campylobacter

High Prevalence and Predominance of the aph(2″)-If Gene Conferring Aminoglycoside Resistance in Campylobacter

Novel plasmid conferring kanamycin and tetracycline resistance in the turkey-derived Campylobacter jejuni strain 11601MD

Practical Value of Food Pathogen Traceability through Building a Whole-Genome Sequencing Network and Database

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