Molecular Genetic Characteristics of Plasmid-Borne mcr-9 in Salmonella enterica Serotype Typhimurium and Thompson in Zhejiang, China

Fan, Jiulun; Cai, Heng; Fang, Youhong; He, Jintao; Zhang, Linghong; Xu, Qingye; Yang, Yuan; Leptihn, Sebastian; Yu, Yunsong; Zhao, Dongdong; Hua, Xiaoting

doi:10.3389/fmicb.2022.852434

Cited by 5 publications

(3 citation statements)

References 35 publications

(41 reference statements)

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“…Our results highlight the problematic nature of measuring colistin resistance in the lab, consistent with several studies that found that the presence of mcr-9 gene is not sufficient to confer colistin resistance [50,74,75]. Nevertheless, over-expression of mcr-9 consistently generates clinically relevant resistance in E. coli [44].…”

Section: Discussionsupporting

confidence: 87%

Plasmid-encoded lactose metabolism and mobilized colistin resistance (mcr-9) genes in Salmonella enterica serovars isolated from dairy facilities in the 1980s

Kröger,

Lerminiaux,

Ershova

et al. 2023

Microbial Genomics

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Horizontal gene transfer by plasmids can confer metabolic capabilities that expand a host cell’s niche. Yet, it is less understood whether the coalescence of specialized catabolic functions, antibiotic resistances and metal resistances on plasmids provides synergistic benefits. In this study, we report whole-genome assembly and phenotypic analysis of five Salmonella enterica strains isolated in the 1980s from milk powder in Munich, Germany. All strains exhibited the unusual phenotype of lactose-fermentation and encoded either of two variants of the lac operon. Surprisingly, all strains encoded the mobilized colistin resistance gene 9 (mcr-9), long before the first report of this gene in the literature. In two cases, the mcr-9 gene and the lac locus were linked within a large gene island that formed an IncHI2A-type plasmid in one strain but was chromosomally integrated in the other strain. In two other strains, the mcr-9 gene was found on a large IncHI1B/IncP-type plasmid, whereas the lac locus was encoded on a separate chromosomally integrated plasmidic island. The mcr-9 sequences were identical and genomic contexts could not explain the wide range of colistin resistances exhibited by the Salmonella strains. Nucleotide variants did explain phenotypic differences in motility and exopolysaccharide production. The observed linkage of mcr-9 to lactose metabolism, an array of heavy-metal detoxification systems, and other antibiotic resistance genes may reflect a coalescence of specialized phenotypes that improve the spread of colistin resistance in dairy facilities, much earlier than previously suspected.

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Section: Discussionsupporting

confidence: 87%

Plasmid-encoded lactose metabolism and mobilized colistin resistance (mcr-9) genes in Salmonella enterica serovars isolated from dairy facilities in the 1980s

Kröger,

Lerminiaux,

Ershova

et al. 2023

Microbial Genomics

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“…Three MDR Salmonella strains were recovered from the strain bank and isolated with Salmonella agar (CHROMagar Company, Paris, France); strains were identified using the Vitek-II system (bioMérieux, Lyon, France). The genomic DNA from each strains was extracted by boiling and freeze-thawing processes, and the resulting supernatant was recovered for use as the PCR template ( Doyle et al, 2012 ; Ding et al, 2020 ; Fan et al, 2022 ).…”

Section: Methodsmentioning

confidence: 99%

Oxford nanopore long-read sequencing enables the generation of complete bacterial and plasmid genomes without short-read sequencing

et al. 2023

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IntroductionGenome-based analysis is crucial in monitoring antibiotic-resistant bacteria (ARB)and antibiotic-resistance genes (ARGs). Short-read sequencing is typically used to obtain incomplete draft genomes, while long-read sequencing can obtain genomes of multidrug resistance (MDR) plasmids and track the transmission of plasmid-borne antimicrobial resistance genes in bacteria. However, long-read sequencing suffers from low-accuracy base calling, and short-read sequencing is often required to improve genome accuracy. This increases costs and turnaround time.MethodsIn this study, a novel ONT sequencing method is described, which uses the latest ONT chemistry with improved accuracy to assemble genomes of MDR strains and plasmids from long-read sequencing data only. Three strains of Salmonella carrying MDR plasmids were sequenced using the ONT SQK-LSK114 kit with flow cell R10.4.1, and de novo genome assembly was performed with average read accuracy (Q > 10) of 98.9%.Results and DiscussionFor a 5-Mb-long bacterial genome, finished genome sequences with accuracy of >99.99% could be obtained at 75× sequencing coverage depth using Flye and Medaka software. Thus, this new ONT method greatly improves base-calling accuracy, allowing for the de novo assembly of high-quality finished bacterial or plasmid genomes without the need for short-read sequencing. This saves both money and time and supports the application of ONT data in critical genome-based epidemiological analyses. The novel ONT approach described in this study can take the place of traditional combination genome assembly based on short- and long-read sequencing, enabling pangenomic analyses based on high-quality complete bacterial and plasmid genomes to monitor the spread of antibiotic-resistant bacteria and antibiotic resistance genes.

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“…However, selective pressure from the overuse or misuse of both antimicrobials has resulted in the emergence of carbapenem- and colistin-resistant Enterobacteriaceae (CRE) ( Nang et al, 2019 ; Octavia et al, 2020 ). Regarding Salmonella isolates, recent studies have demonstrated their resistance to these critical antimicrobial drugs ( Wang et al, 2017 ; Fan et al, 2022 ; Zhang et al, 2022b ).…”

Section: Introductionmentioning

confidence: 99%

Genomic characterization of Salmonella isolated from retail chicken and humans with diarrhea in Qingdao, China

Wang,

Cui,

Liu

et al. 2023

Front. Microbiol.

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Salmonella, especially antimicrobial resistant strains, remains one of the leading causes of foodborne bacterial disease. Retail chicken is a major source of human salmonellosis. Here, we investigated the prevalence, antimicrobial resistance (AMR), and genomic characteristics of Salmonella in 88 out of 360 (24.4%) chilled chicken carcasses, together with 86 Salmonella from humans with diarrhea in Qingdao, China in 2020. The most common serotypes were Enteritidis and Typhimurium (including the serotype I 4,[5],12:i:-) among Salmonella from both chicken and humans. The sequence types were consistent with serotypes, with ST11, ST34 and ST19 the most dominantly identified. Resistance to nalidixic acid, ampicillin, tetracycline and chloramphenicol were the top four detected in Salmonella from both chicken and human sources. High multi-drug resistance (MDR) and resistance to third-generation cephalosporins resistance were found in Salmonella from chicken (53.4%) and humans (75.6%). In total, 149 of 174 (85.6%) Salmonella isolates could be categorized into 60 known SNP clusters, with 8 SNP clusters detected in both sources. Furthermore, high prevalence of plasmid replicons and prophages were observed among the studied isolates. A total of 79 antimicrobial resistant genes (ARGs) were found, with aac(6′)-Iaa, blaTEM-1B, tet(A), aph(6)-Id, aph(3″)-Ib, sul2, floR and qnrS1 being the dominant ARGs. Moreover, nine CTX-M-type ESBL genes and the genes blaNMD-1, mcr-1.1, and mcr-9.1 were detected. The high incidence of MDR Salmonella, especially possessing lots of mobile genetic elements (MGEs) in this study posed a severe risk to food safety and public health, highlighting the importance of improving food hygiene measures to reduce the contamination and transmission of this bacterium. Overall, it is essential to continue monitoring the Salmonella serotypes, implement the necessary prevention and strategic control plans, and conduct an epidemiological surveillance system based on whole-genome sequencing.

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Molecular Genetic Characteristics of Plasmid-Borne mcr-9 in Salmonella enterica Serotype Typhimurium and Thompson in Zhejiang, China

Cited by 5 publications

References 35 publications

Plasmid-encoded lactose metabolism and mobilized colistin resistance (mcr-9) genes in Salmonella enterica serovars isolated from dairy facilities in the 1980s

Plasmid-encoded lactose metabolism and mobilized colistin resistance (mcr-9) genes in Salmonella enterica serovars isolated from dairy facilities in the 1980s

Oxford nanopore long-read sequencing enables the generation of complete bacterial and plasmid genomes without short-read sequencing

Genomic characterization of Salmonella isolated from retail chicken and humans with diarrhea in Qingdao, China

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