Formation, Transmission, and Dynamic Evolution of a Multidrug-Resistant Chromosomally Integrated Plasmid in Salmonella Spp.

Chang, Man-Xia; Zhang, Jing; Zhang, Jin-Fei; Ding, Xiao-Min; Lu, Yang; Zhang, Jie; Li, Ruichao; Jiang, Hongxia

doi:10.3389/fmicb.2022.846954

Cited by 4 publications

(4 citation statements)

References 46 publications

(66 reference statements)

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“…The complete chromosomes and plasmids of these isolates were obtained using a hybrid assembly strategy and single-read analysis, as described in our previous study ( Li et al., 2018 ). According to the assembly results, we found two chromosomally integrated IncHI2 plasmids from isolates SC2016025 and SC2016090 as a similar phenomenon previously reported ( Figures 2A, D ) ( Chang et al., 2022 ). Similar mcr-1 -bearing IncHI2/HI2A plasmids were found in other mcr-1 positive isolates from our investigation including SC2017030, SC2017100, SC2017297 and SC2017167.…”

Section: Resultssupporting

confidence: 90%

The characteristics of mcr-bearing plasmids in clinical Salmonella enterica in Sichuan, China, 2014 to 2017

Sun,

Zhang,

Meng

et al. 2023

Front. Cell. Infect. Microbiol.

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Salmonella is one of the most important zoonotic pathogens and a major cause of foodborne illnesses, posing a serious global public health hazard. The emergence of plasmid-mediated mcr genes in Salmonella has greatly reduced the clinical choice of salmonellosis treatment. The aim of this study was to investigate the plasmid characteristics of mcr-positive Salmonella identified from patients in Sichuan, China during 2014 to 2017 by whole genomes sequencing. In this study, a total of 12 mcr-positive isolates (1.15%, ; mcr-1, n=10; mcr-3, n=2) were identified from 1046 Salmonella isolates using PCR. Further characterization of these isolates was performed through antimicrobial susceptibility testing, conjugation assays, whole genome sequencing, and bioinformatics analysis. The mcr-1 gene in these isolates were carried by three types of typical mcr-1-bearing plasmids widely distributed in Enterobacteriaceae (IncX4, IncI2 and IncHI2). Of note, two mcr-1-harboring IncHI2 plasmids were integrated into chromosomes by insertion sequences. Two mcr-3-bearing plasmids were IncC and IncFIB broad-host-range plasmids respectively. Genetic context analysis found that mcr-1 was mainly located in Tn6330 or truncated Tn6300, and mcr-3 shared a common genetic structure tnpA-mcr-3-dgkA-ISKpn40. Overall, we found that mcr gene in clinical Salmonella were commonly carried by broad-host plasmids and have potential to transfer into other bacteria by these plasmids. Continuous surveillance of MDR Salmonella in humans and investigation the underlying transmission mechanisms of ARGs are vital to curb the current severe AMR concern.

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Section: Resultssupporting

confidence: 90%

The characteristics of mcr-bearing plasmids in clinical Salmonella enterica in Sichuan, China, 2014 to 2017

Sun,

Zhang,

Meng

et al. 2023

Front. Cell. Infect. Microbiol.

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“…The chromosomally integrated plasmid was 330, 232 bp in length and was designated as PSC2020597-sul4-330 k-c ( Figure 1A ). The phenomenon that plasmid was integrated into chromosome have been frequently reported ( Muthuirulandi Sethuvel et al, 2021 ; Shigemura et al, 2021 ; Chang et al, 2022 ), especially in Salmonella , and is commonly mediated by homologous recombination of ISs. We found that PSC2020597-sul4-330 k-c was flanked by IS 1F on chromosome of SC2020597.…”

Section: Resultsmentioning

confidence: 99%

“…By the genetic analysis, we found that sul4 was located on a chromosomally integrated plasmid. However, a previous study demonstrated that chromosomally integrated plasmids could also be transferred to other recipients by conjugation assay ( Chang et al, 2022 ). Here, we verified that there is a circle form of chromosomally integrated plasmid PSC2020597-sul4-330 k-c in some clones of SC2020597 using the inverse PCR method and confirmed by Sanger sequencing ( Supplementary Figure S1 ).…”

Section: Resultsmentioning

confidence: 99%

Emergence of the fourth mobile sulfonamide resistance gene sul4 in clinical Salmonella enterica

Peng,

Deng,

Zou

et al. 2023

Front. Microbiol.

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The fourth mobile sulfonamide resistance gene sul4 has been discovered in many metagenomic datasets. However, there is no reports of it in cultured bacteria. In this study, a sul4 positive clinical Salmonella enterica SC2020597 was obtained by conventional Salmonella isolation methods and characterized by species identification and antimicrobial susceptibility testing. Meanwhile, the genomic DNA was sequenced using both long-read and short-read methods. Following that, the complete genome was analyzed by bioinformatic methods. The sul4 gene in S. enterica SC2020597 differed from the sul4 identified in metagenomic data by one amino acid and could confer full resistance to sulfamethoxazole. Genetic location analysis showed that the sul4 in SC2020597 was carried by a complex chromosomally integrated hybrid plasmid. ISCR20-like was strongly associated with the mobilization of sul4 by core genetic context analysis. To the best of our knowledge, this is the first report of the emergence of sul4 in clinically cultured S. enterica. More important, the sul4 has the potential to spread to other bacteria with the help of mobile elements.

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“…Nonetheless, ISApl1 was lost entirely in mcr-1 plasmids in isolates of E. coli [106,154], Rauoltella planticola [85], and E. fergusonii [163], wherein it was replaced upstream of mcr-1 by pap2-a gene speculated to be compensating for phospholipid metabolism functions altered during LPS modification by COL resistance determinants [245]-and downstream by the nikB gene. This implies that the loss of ISApl1 does not hinder the transmission of the mcr gene.…”

Section: Eastern Asia Chinamentioning

confidence: 99%

Mobile Colistin Resistance (mcr) Gene-Containing Organisms in Poultry Sector in Low- and Middle-Income Countries: Epidemiology, Characteristics, and One Health Control Strategies

et al. 2023

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Mobile colistin resistance (mcr) genes (mcr-1 to mcr-10) are plasmid-encoded genes that threaten the clinical utility of colistin (COL), one of the highest-priority critically important antibiotics (HP-CIAs) used to treat infections caused by multidrug-resistant and extensively drug-resistant bacteria in humans and animals. For more than six decades, COL has been used largely unregulated in the poultry sector in low- and middle-income countries (LMICs), and this has led to the development/spread of mcr gene-containing bacteria (MGCB). The prevalence rates of mcr-positive organisms from the poultry sector in LMICs between January 1970 and May 2023 range between 0.51% and 58.8%. Through horizontal gene transfer, conjugative plasmids possessing insertion sequences (ISs) (especially ISApl1), transposons (predominantly Tn6330), and integrons have enhanced the spread of mcr-1, mcr-2, mcr-3, mcr-4, mcr-5, mcr-7, mcr-8, mcr-9, and mcr-10 in the poultry sector in LMICs. These genes are harboured by Escherichia, Klebsiella, Proteus, Salmonella, Cronobacter, Citrobacter, Enterobacter, Shigella, Providencia, Aeromonas, Raoultella, Pseudomonas, and Acinetobacter species, belonging to diverse clones. The mcr-1, mcr-3, and mcr-10 genes have also been integrated into the chromosomes of these bacteria and are mobilizable by ISs and integrative conjugative elements. These bacteria often coexpress mcr with virulence genes and other genes conferring resistance to HP-CIAs, such as extended-spectrum cephalosporins, carbapenems, fosfomycin, fluoroquinolone, and tigecycline. The transmission routes and dynamics of MGCB from the poultry sector in LMICs within the One Health triad include contact with poultry birds, feed/drinking water, manure, poultry farmers and their farm workwear, farming equipment, the consumption and sale of contaminated poultry meat/egg and associated products, etc. The use of pre/probiotics and other non-antimicrobial alternatives in the raising of birds, the judicious use of non-critically important antibiotics for therapy, the banning of nontherapeutic COL use, improved vaccination, biosecurity, hand hygiene and sanitization, the development of rapid diagnostic test kits, and the intensified surveillance of mcr genes, among others, could effectively control the spread of MGCB from the poultry sector in LMICs.

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Formation, Transmission, and Dynamic Evolution of a Multidrug-Resistant Chromosomally Integrated Plasmid in Salmonella Spp.

Cited by 4 publications

References 46 publications

The characteristics of mcr-bearing plasmids in clinical Salmonella enterica in Sichuan, China, 2014 to 2017

The characteristics of mcr-bearing plasmids in clinical Salmonella enterica in Sichuan, China, 2014 to 2017

Emergence of the fourth mobile sulfonamide resistance gene sul4 in clinical Salmonella enterica

Mobile Colistin Resistance (mcr) Gene-Containing Organisms in Poultry Sector in Low- and Middle-Income Countries: Epidemiology, Characteristics, and One Health Control Strategies

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