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Diversity of Plasmids and Genes Encoding Resistance to Extended-Spectrum β-Lactamase in Escherichia coli from Different Animal Sources.

ABSTRACT: Antimicrobial resistance associated with the spread of plasmid-encoded extended-spectrum β-lactamase (ESBL) genes conferring resistance to third generation cephalosporins is increasing worldwide. However, data on the population of ESBL producing E. coli in different animal sources and their antimicrobial characteristics are limited. The purpose of this study was to investigate potential reservoirs of ESBL-encoded genes in E. coli isolated from swine, beef, dairy, and poultry collected from different regions of the United States using whole-genome sequencing (WGS). Three hundred isolates were typed into different phylogroups, characterized by BOX AIR-1 PCR and tested for resistance to antimicrobials. Of the 300 isolates, 59.7% were resistant to sulfisoxazole, 49.3% to tetracycline, 32.3% to cephalothin, 22.3% to ampicillin, 20% to streptomycin, 16% to ticarcillin; resistance to the remaining 12 antimicrobials was less than 10%. Phylogroups A and B1 were most prevalent with A (n = 92, 30%) and B1 (87 = 29%). A total of nine E. coli isolates were confirmed as ESBL producers by double-disk synergy testing and multidrug resistant (MDR) to at least three antimicrobial drug classes. Using WGS, significantly higher numbers of ESBL-E. coli were detected in swine and dairy manure than from any other animal sources, suggesting that these may be the primary animal sources for ESBL producing E. coli. These isolates carry plasmids, such as IncFIA(B), IncFII, IncX1, IncX4, IncQ1, CollRNAI, Col440I, and acquired ARGs aph(6)-Id, aph(3″)-Ib, aadA5, aph(3')-Ia, bla_CTX-M-15, bla_TEM-1B, mphA, ermB, catA1, sul1, sul2, tetB, dfrA17. One of the E. coli isolates from swine with ST 410 was resistant to nine antibiotics and carried more than 28 virulence factors, and this ST has been shown to belong to an international high-risk clone. Our data suggests that ESBL producing E. coli are widely distributed in different animal sources, but swine and dairy cattle may be their main reservoir.

SUBMITTER: Ibekwe A

PROVIDER: S-EPMC8153348 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Extended-spectrum-beta-lactamase (ESBL)/AmpC-producing Escherichia coli strains are widely found in E. coli isolates from broiler feces, largely due to the presence of the blaCTX-M-1 gene on IncI1 plasmids. Plasmid carriage is theorized to cause fitness loss and thus should decrease under conditions of reduced antibiotic use. However, in vitro studies showed plasmid carriage to increase in the absence of antimicrobials, due to plasmid conjugation. We investigated whether this translates to increased levels of plasmid in the gastrointestinal tracts of chickens, where conjugation rates may be different and subtle differences in growth rates may have a larger impact on colonization. Eight groups of five chickens were orally inoculated at 4 days of age with a 0.5-ml volume containing 106 CFU/ml E. coli cells, of which 0%, 0.1%, 10%, or 100% carried the IncI1 plasmid with the gene blaCTX-M-1 At 13 time points during 41 days, fecal samples were taken from each chicken. E. coli strains with and without plasmids were quantified. Trends in E. coli subpopulations were analyzed using generalized linear mixed models, and population dynamics were studied by fitting to a mechanistic model. Trends in E. coli subpopulations were different between groups rather than between individual chickens, suggesting substantial levels of E. coli exchange between chickens in a group. The IncI1 plasmid carrying blaCTX-M-1 was transferred with conjugation coefficients at levels higher than those observed in vitro Across groups, the plasmids disappeared or were established independently of the initial fraction of plasmid-carrying E. coli, but no major increase occurred as observed in vitro Differences in growth rates were observed, but competitive exclusion of plasmid-carrying variants was counteracted by conjugation.IMPORTANCE Bacteria that produce extended-spectrum beta-lactamases are resistant to an important class of antimicrobials in human and veterinary medicine. Reduction in antibiotic use is expected to decrease the prevalence of resistance. However, resistance genes often lie on plasmids which can be copied and transferred to other bacteria by conjugation, so in vitro resistance was observed to increase in the absence of antimicrobials. We sought to determine whether this also occurs in the chicken gut and if competitive exclusion by similar E. coli variants without the resistance occurred. We studied the excretion of E. coli carrying IncI1 plasmids with the blaCTX-M-1 resistance gene in small groups of broiler chickens, after inoculating the chickens with E. coli suspensions containing different fractions of plasmid-carrying cells. Our results showed little variation between chickens within groups but large differences between groups that were independent of the ratio of variants with and without the plasmid and with persistence or extinction of the plasmid. However, there was no major plasmid increase as observed in vitro We conclude that in vivo studies with sufficient independent replications are important for intervention studies on plasmid-mediated antimicrobial resistance.

Project description:Uropathogenic Escherichia coli (UPEC) is one of the most common causes of urinary tract infections. Here, we report for the first time the whole-genome sequencing (WGS) and analysis of four extended-spectrum β-lactamase (ESBL), UPEC sequence type (ST) 127 isolates that were recovered from patients in five hospitals in Armenia from January to August of 2019. A phylogenetic comparison revealed that our isolates were closely related to each other by their core and accessory genomes, despite having been isolated from different regions and hospitals in Armenia. We identified unique genes in our isolates and in a closely related isolate recovered in France. The unique genes (hemolysin E virulence gene, lactate utilization operon lutABC, and endonuclease restriction modification operon hsdMSR) were identified in three separate genomic regions that were adjacent to prophage genes, including one region containing the TonB-dependent iron siderophore receptor gene ireA, which was only found in 5 other ST127 isolates from the European Nucleotide Archive (ENA). We further identified that these isolates possessed unique virulence and metabolic genes and harbored antibiotic resistance genes, including the ESBL genes blaCTX-M-3 (n = 3), blaCTX-M-236 (n = 1), and blaTEM-1 (n = 1), in addition to a quinolone resistance protein gene qnrD1 (n = 1), which was absent in the ST127 isolates obtained from the ENA. Moreover, a plasmid replicon gene IncI2 (n = 1) was unique to ARM88 of the Armenian isolates. Our findings demonstrate that at the time of this study, E. coli ST127 was a cause of urinary tract infections in patients in different regions of Armenia, with a possibility of cross-country transmission between Armenia and France. IMPORTANCE Whole-genome sequencing studies of pathogens causing infectious diseases are seriously lacking in Armenia, hampering global efforts to track, trace and contain infectious disease outbreaks. In this study, we report for the first-time the whole-genome sequencing and analysis of ESBL UPEC ST127 isolates recovered from hospitalized patients in Armenia and compare them with other E. coli ST127 retrieved from the ENA. We found close genetic similarities of the Armenian isolates, indicating that E. coli ST127 was potentially a dominant lineage causing urinary tract infections in Armenia. Furthermore, we identified unique genes that were horizontally acquired in the clusters of Armenian and French isolates that were absent in other ST127 isolates obtained from the ENA. Our findings highlight a possible cross-country transmission between Armenia and France and the idea that the implementation of WGS surveillance could contribute to global efforts in tackling antibiotic resistance, as bacteria carrying antimicrobial resistance (AMR) genes do not recognize borders.

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Diversity of Plasmids and Genes Encoding Resistance to Extended-Spectrum β-Lactamase in Escherichia coli from Different Animal Sources.

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