Exploring the epidemiology of mcr genes, genetic context and plasmids in Enterobacteriaceae originating from pigs and humans on farms in Thailand

Abstract

Objectives In veterinary medicine, colistin has been widely used as therapeutic and prophylactic agent, and for growth promotion. However, colistin has been re-introduced into treatment of human MDR bacterial infections. We assessed the characteristics and spread of plasmid-borne colistin resistance among healthy pigs, workers with animal-contact and their household members in Thailand. Methods WGS and MIC data of 146 mcr-positive isolates from a cross-sectional One Health study were analysed. Long-read sequencing and conjugation were performed for selected isolates. Results mcr-carrying isolates were detected in 38% of pooled-pig samples and 16% of human faecal samples. Of 143 Escherichia coli and three Escherichia fergusonii, mcr-1, mcr-3, and mcr-9 variants were identified in 96 (65.8%), 61 (41.8%) and one (0.7%) isolate, respectively. Twelve E. coli co-harboured two mcr variants (mcr-1 and mcr-3). Clonal transmission was detected in five out of 164 farms. mcr-1 was mostly harboured by epidemic IncX4 and IncHI1 plasmids (89.9%). Conversely, mcr-3 was harboured by a range of different plasmids. Comparative plasmid studies suggested IncP and IncFII plasmids as possible endemic mcr-3 plasmids in Asian countries. Moreover, mcr-3 was associated with different mobile genetic elements including TnAs2, ISKpn40 and IS26/15DI. Detected genetic signatures (DRs) indicated recent mcr-3 transpositions, underlining the mobilizable nature of the mcr-3 cassette. Conclusions The epidemiology of mcr and the possible evolution of successful plasmids and transposition modules should be carefully monitored. Of special concern is the growing number of different horizontal gene transferring pathways encompassing various transposable modules the mcr genes can be shared between bacteria.

Genetic characterization of multidrug-resistant Escherichia coli harboring colistin-resistant gene isolated from food animals in food supply chain

“…Our study, E. coli harboring mcr-1 and mcr-3 were detected together with ESBL genes ( bla TEM-1B , bla CTX-M-14 and bla CTX-M-55 ). Among them, bla TEM-1B was the most common found in thirteen mcr positive E. coli , these results correlated with previous findings in Thailand that demonstrated the concurrent carriage of mcr-1.1 with bla CTX-M-14 , bla CTX-M-55 , and bla TEM-1B ( Leangapichart et al., 2023 ). Moreover, the coexistence of mcr with ESBL genes in E.coli was report from other studies such as China and Pakistan, E. coli co-harboring mcr with ESBL genes such as bla CTX-M-14 , bla CTX-M-55 , and bla TEM-1B ( Shafiq et al., 2019 ; Shafiq et al., 2022 ).…”

“…These finding resonate with our previously published data, demonstrating mcr-1 carriage by IncX4 and IncI2 replicon in E. coli in humans in Thailand ( Boueroy et al., 2022 ). This supports the notion of mcr gene emergence within specific plasmid groups in Enterobacterales from various reservoirs, including animals, food, environment, and humans ( Boonyasiri et al., 2023 ; Leangapichart et al., 2023 ). Additionally, our experiments revealed the conjugative transfer capacity of IncX4 plasmids harboring mcr-1 .…”

Extended-Spectrum Beta-Lactamase-Producing Escherichia coli in Feces and Wastewater Treatment System in Swine Farms, Thailand

“…The CTX-M-55-producing E. coli and CTX-M-14-producing E. coli were detected at all sampling locations on the swine farms. Result corresponds favorably with several studies conducted in swine in Thailand where blaCTX-M-55, and blaCTX-M-14, were the predominant ESBL gene identified [25,27,28]. Enzymes in these sub-families are widely disseminated and frequently reported [29].…”

Characteristics and genomic epidemiology of colistin-resistant Enterobacterales from farmers, swine, and hospitalized patients in Thailand, 2014–2017

“…We identified E. coli with a new mcr -2 gene variant, mcr-2.3 , among the swine isolates. Typically, mcr genes are found on plasmids; however, co-occurrence of genes on both plasmid and chromosome has been rarely discovered [ 48 – 50 ]. In our study, E. coli harbored mcr -2.3 on the chromosome rather than plasmid, suggesting that mcr -2.3 could have alternative pathways to get into bacterial strains.…”

“…The discovery of an isolate with mcr on both its plasmid and chromosome suggests that the process for stabilizing the mcr -3.21 gene within the bacterial genome is still in progress. Although several studies of E. coli have shown the chromosomal location of mcr -1 and mcr -2 [ 50 , 51 ], the finding of mcr -3.21 on both a plasmid and chromosome in a single isolate has recently been reported in healthy individuals, farmers and swine in Thailand [ 48 , 49 ]. This finding was possible due to opportunity to do long- and short- read sequencing on some of the isolates, and hybrid assembly of these reads allowed a more closed genomes to be analyzed.…”