Dataset Information

Genomic patterns and characterizations of chromosomally-encoded mcr-1 in Escherichia coli populations.

ABSTRACT: The emergence and transmission of the mobile colistin resistance gene (mcr-1) threatened the extensive use of polymyxin antimicrobials. Accumulated evidence showed that the banning of colistin additive in livestock feed efficiently reduce mcr-1 prevalence, not only in animals but also in humans and environments. However, our previous study has revealed that a small proportion of Escherichia coli could continually carry chromosomally-encoded mcr-1. The chromosomally-encoded events, indicated the existence of stabilized heritage of mcr-1 and revealed a potential threat in the antimicrobial stewardship interventions, are yet to be investigated. In this study, we systematically investigated the genetic basis of chromosomally-encoded mcr-1 in prevalence and potential mechanisms of lineage, plasmid, insertion sequence, and phage. Our results demonstrated that the emergence of chromosomally-encoded mcr-1 could originate from multiple mechanisms, but mainly derived through the recombination of ISApl1/Tn6330. We reported a specific transmission mechanism, which is a phage-like region without lysogenic components, could associate with the emergence and stabilization of chromosomally-encoded mcr-1. These results highlighted the potential origin and risks of chromosomally-encoded mcr-1, which could be a heritable repository and thrive again when confronted with new selective pressures. To the best of our knowledge, this is the first study to systematically reveal the genomic basis of chromosomally-encoded mcr-1, and report a specific transmission pattern involved in phage-like region. Overall, we demonstrate the origin mechanisms and risks of chromosomally-encoded mcr-1. It highlights the need of public attention on chromosome-encoded mcr-1 to prevent from its reemergence.

SUBMITTER: Shen C

PROVIDER: S-EPMC7700713 | biostudies-literature | 2020 Nov

REPOSITORIES: biostudies-literature

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Genomic patterns and characterizations of chromosomally-encoded mcr-1 in Escherichia coli populations.

Shen Cong C Zhong Lan-Lan LL Ma Furong F El-Sayed Ahmed Mohamed Abd El-Gawad MAE Doi Yohei Y Zhang Guili G Liu Yang Y Huang Songyin S Li Hong-Yu HY Zhang Liyan L Liao Kang K Xia Yong Y Dai Min M Yan Bin B Tian Guo-Bao GB

Gut pathogens 20201128 1

The emergence and transmission of the mobile colistin resistance gene (mcr-1) threatened the extensive use of polymyxin antimicrobials. Accumulated evidence showed that the banning of colistin additive in livestock feed efficiently reduce mcr-1 prevalence, not only in animals but also in humans and environments. However, our previous study has revealed that a small proportion of Escherichia coli could continually carry chromosomally-encoded mcr-1. The chromosomally-encoded events, indicated the ...[more]

PMID: 33292487

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Project description:The wide distribution of colistin-resistant bacteria in developing countries has become a common phenomenon. To understand the mechanisms underlying their distribution, we studied the mcr genetic background of colistin-resistant Escherichia coli isolates from the fecal microbiota of healthy human residents from a community in Vietnam with a high prevalence of colistin-resistant E. coli with mcr Fifty-seven colistin-resistant isolates were obtained from 98 residents; one isolate was collected from each individual and analyzed for mcr We found that 36.8% of the isolates carried chromosomal mcr-1 Further, 63.2% and 1.8% of the isolates carried mcr-1 on the plasmid and the plasmid/chromosome, respectively. Whole-genome sequencing of genetically unrelated isolates showed that the majority (6 of 7) of the isolates had the chromosomal mcr-1 in a complete ancestral mcr-1 transposon Tn6330, ISApl1-mcr-1-PAP2-ISApl1, which was inserted at various positions on the chromosomes. In addition, the majority (87.5%) of Tn6330 of mcr-1-carrying plasmids (n?=?8) lacked both upstream and downstream ISApl1 transposons. The results obtained in this study indicate that plasmid-to-chromosomal transfer of mcr-1 may have occurred recently in the fecal microbiota of the residents. Additionally, Tn6330 on the chromosome may lose ISApl1 from the transposon during multiplication to gain a more stable mcr-1 state on the chromosome. Stabilization of resistance by the chromosomal incorporation of mcr-1 would be an additional challenge in combating the dissemination of resistant bacteria.IMPORTANCE Elucidation of the mechanism of the wide dissemination of colistin-resistant bacteria in communities of developing countries is an urgent public health issue. In this study, we investigated the genetic background of the colistin resistance gene mcr in E. coli isolates from the fecal microbiota of healthy human residents living in a community in Vietnam with a high prevalence of colistin-resistant E. coli Our study revealed for the first time, a surprisingly high percentage (36.8%) of colistin-resistant E. coli carrying chromosomal mcr-1, the emergence of which may have occurred recently, in the fecal microbiota of the community residents. The mcr-1 transposon on the chromosome may develop into a more stable genotype by the loss of insertion sequences (ISs). Our results are valuable in understanding the mechanism underlying the increasing prevalence of colistin-resistant bacteria within a community.

Project description:Antimicrobial agents are crucial for the treatment of many bacterial diseases in pigs, however, the massive use of critically important antibiotics such as colistin, fluoroquinolones and 3rd-4th-generation cephalosporins often selects for co-resistance. Based on a comprehensive characterization of 35 colistin-resistant Escherichia coli from swine enteric colibacillosis, belonging to prevalent Spanish lineages, the aims of the present study were to investigate the characteristics of E. coli clones successfully spread in swine and to assess the correlation of the in vitro results with in silico predictions from WGS data. The resistome analysis showed six different mcr variants: mcr-1.1; mcr-1.10; mcr-4.1; mcr-4.2; mcr-4.5; and mcr-5.1. Additionally, bla CTX-M- 14, bla CTX-M- 32 and bla SHV- 12 genes were present in seven genomes. PlasmidFinder revealed that mcr-1.1 genes located mainly on IncHI2 and IncX4 types, and mcr-4 on ColE10-like plasmids. Twenty-eight genomes showed a gyrA S83L substitution, and 12 of those 28 harbored double-serine mutations gyrA S83L and parC S80I, correlating with in vitro quinolone-resistances. Notably, 16 of the 35 mcr-bearing genomes showed mutations in the PmrA (S39I) and PmrB (V161G) proteins. The summative presence of mechanisms, associated with high-level of resistance to quinolones/fluoroquinolones and colistin, could be conferring adaptive advantages to prevalent pig E. coli lineages, such as the ST10-A (CH11-24), as presumed for ST131. SerotypeFinder allowed the H-antigen identification of in vitro non-mobile (HNM) isolates, revealing that 15 of the 21 HNM E. coli analyzed were H39. Since the H39 is associated with the most prevalent O antigens worldwide within swine colibacillosis, such as O108 and O157, it would be probably playing a role in porcine colibacillosis to be considered as a valuable subunit antigen in the formulation of a broadly protective Enterotoxigenic E. coli (ETEC) vaccine. Our data show common features with other European countries in relation to a prevalent clonal group (CC10), serotypes (O108:H39, O138:H10, O139:H1, O141:H4), high plasmid content within the isolates and mcr location, which would support global alternatives to the use of antibiotics in pigs. Here, we report for first time a rare finding so far, which is the co-occurrence of double colistin-resistance mechanisms in a significant number of E. coli isolates.

Dataset Information

Genomic patterns and characterizations of chromosomally-encoded mcr-1 in Escherichia coli populations.

Publications

Genomic patterns and characterizations of chromosomally-encoded mcr-1 in Escherichia coli populations.

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