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. 2026 Mar 10;83(4):238. doi: 10.1007/s00284-026-04812-6

Polymyxin-Resistant Escherichia coli Found in Vegetables from Brazil: An Emerging Public Health Concern

Arthur Bossi do Nascimento 1, Bruno Henrique Dias de Oliva 1, Gustavo Henrique Migliorini Guidone 1, Luana Carvalho Silva 1, Luana Karolyne Salomão de Almeida 1, Renata Katsuko Takayama Kobayashi 2, Sergio Paulo Dejato Rocha 1,3,✉
PMCID: PMC12975781  PMID: 41807726

Abstract

Vegetables are essential components of a healthy diet and are frequently consumed raw, which can facilitate the transmission of pathogens such as Escherichia coli. In addition to causing infections, E. coli can transfer resistance genes, such as mcr-1 (mobilized colistin resistance), to other microorganisms, conferring resistance to polymyxins. This study aimed to phenotypically and genotypically characterize polymyxin-resistant E. coli strains isolated from vegetables sold in Brazil. Among 514 samples analyzed, 10 E. coli strains exhibited polymyxin resistance: 5 from lettuce, 2 from chicory, and 3 from watercress, cabbage, and arugula. Broth microdilution revealed minimum inhibitory concentrations (MICs) of 4 µg/mL for eight isolates and 8–16 µg/mL for the remaining two. Antimicrobial susceptibility testing indicated a phenotype consistent with AmpC β-lactamase production, as seven isolates were resistant to cefoxitin, and whole-genome sequencing confirmed the presence of blaAmpC genes. Several isolates also showed resistance to other β-lactams, fosfomycin, and trimethoprim-sulfamethoxazole. Four strains successfully transferred polymyxin resistance via conjugation, suggesting plasmid-mediated gene transfer. Genome sequencing identified multiple sequence types (STs), with ST48 being the most prevalent, and detected two plasmids carrying the mcr-1 gene. Phylogenetic analysis revealed that these strains were related to diverse sources, including environmental and animal reservoirs. This study reports the presence of polymyxin-resistant E. coli in vegetables in Brazil, highlighting the zoonotic risk and the potential spread of resistance genes through mobile plasmids. These findings emphasize the need for continued surveillance of fresh produce to limit the dissemination of antimicrobial resistance and protect public health.

Introduction

Vegetables are essential components of a healthy and balanced diet. In recent years, global consumption of these foods has increased due to the growing promotion of healthier lifestyles [1]. However, they are often consumed fresh without undergoing prior processing to ensure the effective removal or inactivation of contaminants, such as chemical residues or pathogenic microorganisms [2].

Among the microorganisms that can contaminate vegetables, Escherichia coli is a notable Gram-negative bacterium of the Enterobacteriaceae family. It is commonly found in the gastrointestinal tracts of humans and homeothermic animals as part of their natural intestinal microbiota [3]. However, certain strains of E. coli are pathogenic and can cause infections in the urinary tract, digestive system, and bloodstream [1].

E. coli transmission occurs primarily through the consumption of contaminated foods, particularly undercooked meats and raw vegetables [4]. Of particular concern is this microorganism’s remarkable capacity to acquire antibiotic resistance genes, including mcr-1, which confers polymyxin resistance through horizontal gene transfer [5]. The spread of these resistance genes is facilitated by mobile genetic elements, notably transposons and multidrug-resistant (MDR) plasmids [6].

The mcr-1 gene was first identified in November 2015 in China, where it was detected in E. coli isolates from pigs in slaughterhouses and retail meat products [7]. Other studies have also reported the presence of the mcr-1 gene in E. coli isolated from vegetable samples in various countries, including South Korea, China, and Portugal, highlighting its widespread dissemination across diverse sources [8–10]. Prior to this discovery, polymyxin resistance was understood to occur exclusively through chromosomal mechanisms [11].

Polymyxins are cyclic lipopeptide antibiotics that were first isolated from Bacillus polymyxa in 1947. They currently represent one of the last remaining therapeutic options against MDR Gram-negative pathogens, such as Klebsiella pneumoniae, Pseudomonas aeruginosa, and Acinetobacter baumannii. Their bactericidal activity mainly involves electrostatic binding to lipopolysaccharides in the bacterial outer membrane, followed by the insertion of the hydrophobic acyl tail, which disrupts the membrane’s integrity and causes cell lysis. In addition to their significant clinical relevance, the rise of polymyxin-resistant strains poses a growing clinical problem, resulting in substantial economic burden through prolonged hospitalizations, higher treatment costs, and increased mortality rates linked to hard-to-treat infections. The presence of polymyxin-resistant E. coli in vegetables heightens this concern, since contaminated produce can serve as a carrier for the environmental spread of resistance genes, thereby posing threats to food safety and public health [11, 12].

This study evaluated the prevalence of polymyxin-resistant E. coli in 514 vegetable samples collected from the Londrina region of Paraná State, Brazil. We conducted phenotypic characterization of antimicrobial resistance patterns and investigated the potential horizontal transfer of polymyxin resistance genes through conjugation assays. Additionally, we performed whole-genome sequencing to comprehensively analyze the genotypic profiles of these resistant strains.

Materials and Methods

Study Design and Microbiological Analyses

This study utilized 514 vegetable samples. The sampling strategy aimed to cover the majority of retail outlets selling these vegetables in the Londrina region, in order to ensure representative coverage of local distribution. Sampling sites were randomly selected across different commercial establishments, including street markets and grocery stores. All vegetable samples were processed on the same day of purchase to minimize potential alterations due to storage. Bacterial isolates were obtained between October 2022 and February 2023 from the city of Londrina, Brazil. Bacteria were isolated from vegetables following a modified methodology based on [13]. Initially, 25 g of each vegetable sample were placed in a sterile flask containing 225 mL of buffered peptone water, homogenized for 5 min, and incubated for 24 h at 37 °C. Subsequently, a 1 mL aliquot of the peptone water was transferred to 9 mL of Brain Heart Infusion (BHI) broth (Difco™) supplemented with polymyxin at its minimum inhibitory concentration (MIC) of 4 µg/mL [14] and incubated again for 24 h at 37 °C. The culture was then plated on MacConkey agar (Difco™) and incubated for an additional 24 h at 37 °C. Colonies displaying a reddish coloration and concave morphology were biochemically screened using EPM, MILi (PROBAC™), and Simmons citrate (Difco™) tests for confirmation. E. coli ATCC 25,922 was processed in parallel with the test samples and used as a positive control for the enrichment and isolation procedures, confirming that the culture media and incubation conditions supported target growth. In addition, an uninoculated enrichment broth served as a negative control to monitor potential contamination of media or reagents. Each of the 514 vegetable samples was processed and analyzed individually rather than as pooled groups, ensuring that potential E. coli contamination and resistance profiles were independently assessed for each sample.

Vegetable samples were collected in equal proportions from two cultivation systems: conventional soil-based farming and hydroponic production. The samples represented seven vegetable varieties: lettuce (Lactuca sativa), arugula (Eruca sativa), chicory (Cichorium intybus), watercress (Nasturtium officinale), spinach (Spinacia oleracea), cabbage (Brassica oleracea var. capitata), and escarole (Cichorium endivia).

A total of 100 lettuce, 90 spinach, 80 cabbage, 80 arugula, 65 escarole, 54 watercress, and 45 chicory samples were analyzed. All samples were collected from retail markets. During each sampling visit, between 15 and 16 samples were obtained.

Phenotypic Characterization of Antimicrobial Resistance

Broth Microdilution Assay

The MIC was determined via broth microdilution, following Clinical and Laboratory Standards Institute (CLSI) guidelines [14]. Experiments were performed in triplicate using Mueller-Hinton broth (MHB; Difco™) supplemented with four polymyxin concentrations (2 µg/mL, 4 µg/mL, 8 µg/mL and 16 µg/mL). Bacterial growth was assessed visually, and the MIC was defined as the lowest polymyxin the concentration that completely inhibited growth, and resistance was confirmed based on CLSI breakpoints [14]. MIC assays were performed using the reference strain E. coli ATCC 25,922 as a quality control, in accordance with CLSI guidelines [14].

This method is recommended by CLSI as the reference standard for polymyxins because disk diffusion is unreliable due to the poor diffusion of these molecules in agar media. For the other antimicrobials tested, disk diffusion was used for routine susceptibility testing, also in accordance with CLSI guidelines.

Antimicrobial Susceptibility

The antimicrobial susceptibility of E. coli isolates obtained from vegetable samples was analyzed using the disk diffusion technique on Mueller-Hinton agar (MHA) (Difco™) according to [15]. Prior to susceptibility testing, bacterial suspensions were adjusted to a turbidity equivalent to a 0.5 McFarland standard (approximately 1 × 10⁸ CFU/mL). Disk diffusion results were interpreted according to the breakpoints established by the CLSI [14]. Isolates were classified as susceptible or resistant based on the zone diameter criteria specified for each antimicrobial agent. To assess the extended-spectrum β-lactamase (ESBL) production, the disk approximation technique was performed following CLSI guidelines [14]. The antimicrobials recommended by CLSI were used in the test [15]. A total of 19 antimicrobials, commonly used in human and veterinary medicine, were tested, including: Piperacillin-Tazobactam (PPT), Amoxicillin-Clavulanate (AMC), Ampicillin (AMP), Cephalothin (CFL), Cefoxitin (CFO), Ceftazidime (CAZ), Ceftriaxone (CRO), Ceftiofur (CTF), Cefepime (CPM), Aztreonam (ATM), Ertapenem (ERT), Enrofloxacin (ENO), Levofloxacin (LEV), Fosfomycin (FOS), Trimethoprim-Sulfamethoxazole (SXT), Norfloxacin (NOR), Gentamicin (GEN), Nalidixic Acid (NAL), and Ciprofloxacin (CIP). Disk diffusion assays were also validated using E. coli ATCC 25,922 as the quality control strain [14].

Conjugation Transfer Assay

The conjugation ability of the isolates was evaluated using a modified methodology based on [16]. The recipient strain used was E. coli J53 (F⁻ met⁻ pro⁻ Aziᴿ), a plasmid-free laboratory strain commonly used in conjugation experiments due to its inherent resistance to sodium azide, which facilitates the efficient selection of transconjugants.

For the assay, test tubes containing Luria-Bertani (LB) broth (Difco™) supplemented 150 µg/mL sodium azide and 4 µg/mL polymyxin B were prepared. E. coli J53 was inoculated into the sodium azide-containing tubes, while the polymyxin-containing tubes were inoculated with the 10 E. coli donor isolates from this study. All samples were incubated for 24 h at 37 °C. After growth, 20 µL of the donor culture and 180 µL of the recipient culture were combined in 96-well plates at a 1:10 donor-to-recipient ratio and incubated for 24 h at 37 °C (the mating mixture). Subsequently, 100 µL of the resulting culture was transferred to a MacConkey agar (Difco™) plate containing 150 µg/mL sodium azide and 4 µg/mL polymyxin. (selective medium). The liquid was spread using a Drigalski loop and incubated for an additional 24 h at 37 °C. Conjugation was confirmed by colony growth on the selective plates (indicating transconjugants), and further verification was performed by transferring a colony to a test tube containing sodium azide and polymyxin at the same concentrations.

To ensure reproducibility, a negative control was included by co-incubating the recipient strain with a non-conjugative donor isolate under the same experimental conditions. No colony growth was observed on selective media, confirming that transfer events were not due to spontaneous resistance or contamination.

The conjugation frequency was calculated as the ratio of transconjugants to donor cells (T/D), determined by plating serial dilutions of the mating mixtures on selective and non-selective agar to quantify donor, recipient, and transconjugant colonies (expressed as CFU/mL).

Whole-Genome Sequencing Analysis

Genomic DNA was extracted using the DNeasy Blood & Tissue Kit (Qiagen, Hilden, Germany) according to the manufacturer’s instructions. DNA concentration and purity were assessed using a NanoDrop spectrophotometer (Thermo Fisher Scientific, USA). Whole-genome sequencing of the 10 selected isolates was performed on the Illumina MiSeq platform (Illumina, San Diego, CA) with 2 × 250 bp paired-end reads. Read quality and sequencing depth were evaluated, with average genome coverage ranging from approximately 15× to 30×. All assembled genomes have been deposited in the NCBI Sequence Read Archive under BioProject accession number PRJNA1173088 (https://www.ncbi.nlm.nih.gov/bioproject/PRJNA1173088).

Assembly and Annotation

Read quality control was performed using Trimmomatic v0.39 (available at https://github.com/usadellab/Trimmomatic) and genome assembly was carried out using SPAdes 4.0.0 (available at https://github.com/ablab/spades). Genome Annotation was conducted using Prokka v1.14.5 (available at https://github.com/tseemann/prokka). Resistance genes and plasmids were identified using ABRIcate v1.0.0 (available at https://github.com/tseemann/abricate). Serotyping was determined using ECTyper v1.0.0 [17], and Multi-Locus Sequence Typing (MLST) was determined using PubMLST [18].

Phylogenetic Analysis and wgMLST

For the phylogenetic analysis of strains carrying plasmids with the mcr gene, a minimum spanning tree (MST) was generated in EnteroBase using the MSTree V2 algorithm, incorporating the whole-genome Multi-Locus Sequence Typing (wgMLST) profiles of selected strains [19]. A total of 277 publicly available E. coli genomes with corresponding sequence types (STs) and relevant epidemiological metadata (source of origin, collection year, and country) were included for comparative purposes. Clermont phylogenetic group determination was also performed using ClermonTyping v1.4.1 (available at https://github.com/A-BN/ClermonTyping) to classify isolates according to the E. coli phylogroup scheme. All figures and phylogenetic trees were generated and annotated using the Interactive Tree of Life software, iTOL v6 [20].

Characterization of mcr-Carrying Plasmids

To construct the plasmid comparison image, a NCBI-BLAST search was performed using the sequences of mcr genes present in plasmids AP005147 and AP010962. Among the 100 plasmids analyzed, those containing the mcr gene were selected for comparative analysis. The image was generated using the BRIG software v0.95 (available at https://sourceforge.net/projects/brig) [21].

Statistical Analysis

Statistical analyses were performed using R version 4.3.2. Associations between categorical variables were evaluated using Pearson’s chi-square test or Fisher’s exact test, as appropriate. A p-value < 0.05 was considered statistically significant.

Results

Isolation, Identification, and Bacterial Sampling

We analyzed a total of 514 vegetable samples, which included 100 lettuce, 90 spinach, 80 cabbage, 80 arugula, 65 escarole, 54 watercress, and 45 chicory samples. Of these, 283 (55%) were sourced from soil-based cultivation and 231 (45%) from hydroponic systems. Overall, we recovered 10 isolates (2%) of polymyxin-resistant E. coli: 5 from lettuce (5.0%), 2 from chicory (4.4%), and 1 each from watercress (1.9%), cabbage (1.3%), and arugula (1.3%). Regarding cultivation methods, 6 (60%) were from soil-based cultivation and 4 (40%) from hydroponic cultivation (Fig. 1). The identification of E. coli was performed using biochemical tests and confirmed by molecular identification of the 16S rRNA gene during the annotation stage of the sequenced genome.

Fig. 1.

Fig. 1

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Graph illustrating the data on the origin of the samples and their phenotypic characteristics. Piperacillin + Tazobactam (PPT), Amoxicillin + Clavulanate (AMC), Ampicillin (AMP), Cephalothin (CFL), Cefoxitin (CFO), Ceftazidime (CAZ), Ceftriaxone (CRO), Ceftiofur (CTF), Cefepime (CPM), Aztreonam (ATM), Ertapenem (ERT), Enrofloxacin (ENO), Nalidixic Acid (NAL), Ciprofloxacin (CIP), Levofloxacin (LEV), Norfloxacin (NOR), Gentamicin (GEN), Fosfomycin (FOS), Sulfamethoxazole (SXT)

Antimicrobial Susceptibility Testing

All isolates underwent MIC testing to confirm polymyxin resistance. Among the 10 isolates, 8 showed inhibition of growth at a concentration of 4 µg/mL, while the remaining two displayed inhibition of growth at 8 µg/mL and 16 µg/mL, respectively, and were classified as resistant based on CLSI criteria (Fig. 1).

As presented in Fig. 1, all isolates demonstrated resistance to AMC, AMP, and CFL. Additionally, eight isolates were resistant to CFO, seven to FOS, six to CAZ, five to CRO and CTF, and three isolates to ATM, CPM, and SXT. Finally, none of the isolates exhibited resistance to CIP, ENO, ERT, GEN, LEV, NAL, NOR, and PPT.

Conjugation Transfer Assay

The conjugation assay was performed, and four out of the 10 isolates successfully transferred the plasmid to the recipient strain E. coli J53. The resulting transconjugants were inoculated into a new medium containing polymyxin and sodium azide to confirm plasmid transfer and resistance to both antimicrobials (Fig. 1). These four conjugative isolates corresponded to the same strains later identified by whole-genome sequencing as carrying mcr-1-harboring plasmids (LBUEL-ECV03, LBUEL-ECV05, LBUEL-ECV07, and LBUEL-ECV08).

Whole-Genome Sequencing and Phylogenetic Analysis

Genomic analysis revealed diversity among the 10 studied strains in terms of Clermont phylotyping, with the presence of groups B1 and A. Similar variations were observed in serotypes, which displayed distinct classifications. Regarding sequence types (STs), three strains shared ST48 (belonging to the ST10 clonal complex), while the others exhibited greater diversity.

With respect to genes associated with polymyxin resistance, the chromosomal pmr gene was present in all strains, whereas four carried the plasmid-borne mcr gene. Among the identified plasmids, two (AP010962 and AP005147) harbored the mcr-1 gene and were detected in four of the analyzed strains (Fig. 2). The analysis of antimicrobial resistance genes, based on phenotypic results, revealed a similar profile among the strains, with the same genes identified in most of them. Additionally, different efflux pump genes were observed, with the acrAB-TolC and emrAB-TolC complexes present in all strains (Fig. 2).

Fig. 2.

Fig. 2

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Genes related to antimicrobial resistance and efflux pumps, Clermont Phylotyping, Serotype, ST, Clonal Complex, Resistance Genes/Polymyxin, Inc/Plasmid Group of E. coli strains isolated from vegetables in Londrina, PR

Two plasmids containing the mcr-1 gene were identified: p0111_1__AP010962 and IncI1I(Alpha)_1__AP005147. (A) The circular plasmid AP010962, measuring 97,897 bp (Fig. 3), exhibited 100% coverage and 98.64% identity. (B) In contrast, the circular plasmid AP005147, measuring 120,826 bp (Fig. 3), showed 93.66% coverage and 88.97% identity. BLAST analysis indicated that AP005147 is related to plasmids found in Salmonella enterica and E. coli carrying the mcr-1 gene, isolated from human samples. Conversely, AP010962 was associated with E. coli plasmids from various sources, including swine, poultry, and humans. Other plasmids identified, including KU674895, M28829, NC_009781, and AP002527, were analyzed but did not contain genes related to polymyxin resistance (Fig. 2). Finally, both plasmids exhibited genes associated with mobilization, such as repA, parA, parB, traV, traU, traG, traI, traJ, traC, traM, traN, traO, traP, traQ, traR, traE, and traF.

Fig. 3.

Fig. 3

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(A) Comparative analysis of plasmids carrying the mcr-1 gene. The reference plasmid is E. coli pO111_2 (AP010962), shown in the innermost ring. Homology with other E. coli plasmids is represented in the outer rings: p2017-19-1CC (AP027855), p.E166-P1 (CP032067), pHeN100_02 (CP044439), p1506-2 (CP059290), pCPWWCT-p0111 (CP076576), and p779-3 (CP086223). (B) Comparative analysis of plasmids carrying the mcr-1 gene. The reference plasmid is S. enterica R64 (AP005147), shown in the innermost ring. Homology with other plasmids is shown in the outer rings: S. enterica PNUSAS070160_1 (CP092295), PNUSAS041145_1 (CP092298), and E. coli pEco_M22546_100 (CP133928)

Phylogenetic tree analysis revealed that the ST48 strains in this study—specifically LBUEL-ECV03 (ESC_PC5539AA_AS), LBUEL-ECV07 (ESC_RC2349AA_AS), and LBUEL-ECV05 (ESC_PC5540AA_AS) were associated with different sources. Strains LBUEL-ECV03 and LBUEL-ECV07 were related to isolates from the environment and chickens, whereas strain LBUEL-ECV05 showed a significant relationship with isolates from cattle and chickens (Fig. 4). A more detailed analysis of closely related strains revealed a wide geographic distribution among the genomes. Furthermore, isolates were associated with a variety of sources, including humans and other animals (Fig. 5).

Fig. 4.

Fig. 4

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Phylogeny of E. coli strains isolated from vegetables carrying the mcr-1 gene. wgMLST of 277 E. coli strains of ST48, isolated between 2022 and 2024. A minimum spanning tree was constructed with strains from the EnteroBase database using the MSTree V2 tool. Each square represents the strain’s origin, while the stars indicate the strains from this study

Fig. 5.

Fig. 5

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Detailed view of the phylogenetic tree shown in Fig. 5, highlighting E. coli ST48 strains that are genetically closest to those sequenced in this study (indicated by stars). Inner ring colors represent the country of origin, and outer ring colors indicate the source of isolation

Statistical Analysis

No statistically significant associations were observed between E. coli occurrence and either vegetable type or cultivation system (p = 0.11 and p = 1.00, respectively). Although lettuce and chicory showed the highest raw counts among the positive samples, these differences were not statistically significant. Notably, the relatively small number of positive samples (n = 10) may have limited the statistical power to detect small group differences. Therefore, the observed patterns should be interpreted with caution and confirmed through larger-scale studies designed to better elucidate potential associations.

Discussion

Vegetables are widely recognized as an important component of a healthy diet. However, their frequent consumption in raw form may facilitate their role as vehicles for pathogenic microorganisms. Among those commonly associated with fresh produce, E. coli and S. enterica have been implicated in multiple foodborne outbreaks worldwide [22, 23]. In the present study, E. coli was detected across various types of vegetables, consistent with findings reported elsewhere [24]. This observation suggests the absence of a strict association between this microorganism and specific vegetable types. However, a higher prevalence may be observed in certain types, such as lettuce [10]. Among the analyzed samples, lettuce and chicory exhibited the highest prevalence of E. coli isolates in our dataset, with 5/100 and 2/45 isolates found, respectively. According to Fisher’s exact test, this pattern was not statistically significant (p = 0.11), implying that the variation observed among vegetable types is probably due to sampling restrictions rather than revealing actual differences in contamination risk.

Studies in countries including China, South Korea, Portugal, and the United Kingdom have identified E. coli carrying mcr from vegetables and animal products, underscoring the worldwide spread of polymyxin resistance [10, 31]. Despite the limited availability of data from South America, only a few studies have examined isolates at both the phenotypic and genomic levels [34, 35]. This study fills this gap by offering the first detailed description of mcr-positive E. coli from vegetables in Brazil, encompassing phylogenetic and plasmid analyses. These results contribute to a better comprehension of the regional patterns of antimicrobial resistance and provide new evidence on the potential for foodborne dissemination of polymyxin-resistant E. coli in Brazil.

Vegetable cultivation can be carried out using different methods. In soil-based cultivation, vegetables are grown directly in the soil until harvest. Conversely, in hydroponic cultivation, vegetables lack soil contact; instead, their roots are immersed in an aqueous solution containing essential nutrients for plant development [25]. The isolates in the present study were recovered from both cultivation systems. Studies on E. coli O157:H7 have shown that this bacterium can penetrate plant roots and colonize the plant in both hydroponic and soil-based cultivation systems. In both cases, the colonization process is hypothesized to originate at sites of root damage [26, 27]. Consistent with these findings, we observed no substantial link between the cultivation system type and the E. coli isolation frequency (Fisher’s exact test, p = 1.00). This suggests that contamination is likely influenced by external environmental or handling factors rather than the specific cultivation method.

Polymyxin-resistant bacteria pose a serious threat to global health, significantly impacting the treatment of MDR bacterial infections [11]. The situation worsened by the presence of polymyxin-resistant microorganisms in vegetables. Despite differences in isolation methodologies, studies conducted in various countries have reported similar findings in vegetable samples, including South Korea (7/1474), China (2/712), and Portugal (1/333) [8, 9, 28]. Although the prevalence is low, its widespread detection across different countries is notable, highlighting the dissemination potential of polymyxin resistance.

Our findings are comparable to reports in China and Portugal, which documented the presence of mcr-positive E. coli in retail meat and environmental samples, suggesting that fresh produce may also serve as a reservoir for these genes [10, 28, 29]. The detection of mcr-1 in Brazilian vegetables implies that resistance factors are not confined to specific geographical areas and can spread globally through the food supply system. This observation aligns directly with findings from the One Health approach in Europe and Asia, emphasizing the interconnectedness of human, animal, and environmental health in the context of antimicrobial resistance.

The mcr-1 gene, responsible for polymyxin resistance, is located on plasmids and has been reported in bacteria such as E. coli, Klebsiella pneumoniae, and S. enterica [30]. Various plasmids containing this gene have been identified and isolated from diverse sources, including humans, animal products, and vegetables, in countries such as China, Denmark, and the United Kingdom [10, 31]. In our study, we identified two mobile plasmids carrying the mcr-1 gene, capable of transferring to other bacterial cells through conjugation. This mechanism facilitates the rapid dissemination of this gene to other bacteria and environments, contributing significantly to the spread of resistance and increasing the risk of its global dissemination [29].

Bacteria producing blaAmpC pose a major challenge for treating bacterial infections. This issue becomes even more concerning when bacteria carry both blaAmpC genes and polymyxin resistance genes. Although reports of the concurrent occurrence of these genes are scarce, their presence has been observed in different countries, including Estonia and Spain [32, 33]. In Brazil, E. coli carrying both mcr-1 and blaCTX−M genes has been reported in isolates from humans and cattle [34, 35]. However, there are no existing records of vegetable-derived isolates carrying both mcr-1 and blaAmpC genes in Brazil. In this study, no specific confirmatory test for AmpC production was performed; however, seven isolates exhibited resistance to cefoxitin, which is commonly associated with the AmpC β-lactamase phenotype. Crucially, whole-genome sequencing confirmed the presence of blaAmpC genes among these isolates.

Fosfomycin is a widely used antimicrobial for treating bacterial infections, particularly urinary tract infections. Studies have demonstrated the presence of bacteria harboring genes conferring resistance to both fosfomycin and polymyxin [36, 37]. The fosA gene, for example, is the most prevalent and has been identified in various contexts, such as supermarkets in Egypt, animals in France, and chickens in Malaysia [38, 39]. In contrast, the efflux pump mdtG/yceE, which, when overexpressed, confers fosfomycin resistance, has not yet been reported alongside polymyxin resistance genes [40]. Fosfomycin resistance is particularly concerning as it eliminates one of the available treatment options for infections frequently caused by E. coli. Moreover, the presence of strains with a broad arsenal of resistance genes exacerbates the situation, rendering these infections potentially lethal due to a lack of effective therapeutic options.

Efflux pumps function by expelling toxic substances, including clinically relevant antimicrobials, from bacterial cells into the external environment. Within the Enterobacteriaceae family, the primary efflux pumps are AcrAB-TolC, OqxAB-TolC, EmrAB-TolC, and MacAB-TolC. These contribute to resistance against various antimicrobial agents, including β-lactams, chloramphenicol, fluoroquinolones, and tetracyclines. Most studies on these efflux pumps have focused on clinical strains [40, 41], with few examining their occurrence in vegetables. However, efflux pumps like EmrAB have been identified in vegetable samples [42]. Our study revealed that all strains contained the AcrAB-TolC and EmrAB-TolC complexes, suggesting that the overexpression of these mechanisms may confer resistance to multiple antimicrobial classes. Additionally, this resistance might be linked to compounds such as detergents, disinfectants, and widely used biocides. The presence of these strains in vegetables is highly problematic because common disinfection methods rely on these compounds, which may consequently become ineffective. Consequently, the risk of contamination by these microorganisms increases, threatening food safety.

Another alarming factor is the presence of these pathogens in vegetables, which increases the risk of cross-contamination during food handling. Such contamination can facilitate the spread of resistant bacteria in various situations. During food processing in kitchens, improper handling is a major factor, with hands, knives, and cutting boards serving as potential contamination sources [43]. The majority of contamination, however, often occurs on cutting boards where food is processed, particularly when the same utensil is used for different foods without proper sanitation. A common example involves cutting raw meat (e.g., chicken) and then using the same board for cutting vegetables without prior cleaning. According to [44], approximately 40% of foodborne contamination occurs in the kitchen during food handling.

Beyond vegetable sources, meat products represent well-established reservoirs of antimicrobial-resistant bacteria and resistance genes, which are frequently associated with mobile plasmids. The co-occurrence of resistant bacteria in meat and fresh produce increases the risk of cross-contamination during food handling, particularly within domestic kitchen environments. This scenario may facilitate the dissemination and co-selection of resistant strains throughout the food chain, further underscoring the One Health perspective [45].

The most prevalent incompatibility groups (Inc) among plasmids carrying the mcr-1 gene are IncI2, IncX4, and IncHI2. Among these, IncX3, IncX4, and IncHI2 plasmids are more frequently found in vegetables. In contrast, IncI1 and p0111 group plasmids carrying the mcr-1 gene have been reported less frequently [46]. Notably, our study revealed the presence of mcr-1 carrying plasmids from the less frequently reported IncI1 and p0111 groups. Generally, these plasmids are frequently associated with genes encoding ESBL and are commonly isolated from humans, cattle, and chickens. However, in our study, the plasmids found did not present genes related to the ESBL profile. According to the literature, the mcr-1 gene is believed to propagate across different plasmids rather than via a predominant clone [47]. This mechanism could facilitate the emergence of new plasmids capable of spreading polymyxin resistance, thus complicating epidemiological monitoring.

Multilocus sequence typing (MLST) is a widely used bacterial adopted method for the molecular identification and classification of bacterial strains, serving as an important tool in the study of bacterial populations. ST48 has been reported across diverse geographical regions and sources, including hospitals and poultry in China, water in France, and birds in the Czech Republic. Furthermore, bacteria belonging to this ST may harbor multiple resistance genes, such as blaKPC, blaNDM, blaCTX−M, mcr-1, and qnrS1 [48–50]. Our study demonstrated close phylogenetic relationship between the ST48 strains isolated from vegetables, cattle, poultry, and various environmental sources. This finding indicates that vegetables may act as an interface linking environmental, animal, and human reservoirs of ST48, thereby facilitating its circulation across these interconnected niches and underscoring the One Health framework. Moreover, genomes with high similarity were distributed across various countries, including the United States, Switzerland, and Thailand. The diversity of sources associated with ST48 suggests that this bacterial group is widely disseminated and not restricted to a specific origin. The presence of multiple resistance genes in bacteria of this ST, combined with its broad distribution across different countries and sources, underscores its significant zoonotic risk. This concern is amplified when such microorganisms are detected in foods typically consumed raw, such as vegetables, which may facilitate their dissemination through the food chain.

Phylogenetic analysis highlighted the close connection between the Brazilian ST48 isolates and environmental and animal strains found in Europe, North America, and Asia, supporting the idea that this lineage has spread internationally. Research from China and France has found comparable connections between foodborne and clinical isolates, with ST48 being associated with poultry and drinking water [49, 50]. This suggests that this lineage circulates across various ecological niches and may facilitate the exchange of resistance genes between non-clinical and clinical settings, fully aligning with the One Health concept.

These results collectively underscore the necessity for coordinated surveillance efforts that cover food, animals, and the environment (the One Health approach) to gain a deeper understanding of the spread of plasmid-mediated polymyxin resistance. Future studies should specifically investigate possible channels of contamination from farm to consumer and evaluate the longevity of mcr-carrying plasmids in the environment. The genomic surveillance of fresh produce should be expanded to offer valuable insights for reducing the spread of MDR bacteria and informing effective public health strategies in Brazil.

Conclusion

In our study, we identified the presence of polymyxin resistant E. coli in vegetables in Brazil, carrying both plasmid-mediated and chromosomal resistance genes. This finding highlights the potential risk posed by these pathogens in such food products and reinforces the need for continuous monitoring. Crucially, most analyzed strains exhibited resistance to cefoxitin, consistent with the AmpC β-lactamase phenotype, and whole-genome sequencing confirmed the presence of blaAmpC genes among these isolates. The coexistence of blaAmpC and polymyxin resistance may further limit treatment options for infections caused by these bacteria. The detection of two mobile plasmids carrying the mcr-1 gene, confirmed to be conjugative, underscores the high potential for the dissemination of this critical resistance gene. Genome analysis revealed that the strains belong to ST48, showing an association with different sources and countries, which highlights the significant zoonotic risk related to these bacteria. These findings emphasize the necessity of monitoring these food products and underscore the need for further studies to investigate the source of contamination in vegetables and mitigate the spread of MDR E. coli.

Authors contribution

Arthur Bossi do Nascimento: Conceptualization, Methodology, Software. Bruno Henrique Dias de Oliva: Software, Data curation. Gustavo Henrique Migliorini Guidone: Visualization, Investigation. Luana Carvalho Silva: Formal analysis, Methodology. Luana Karolyne Salomão de Almeida: Investigation, Data Curation. Renata Katsuko Takayama Kobayashi: Funding acquisition, Writing- Reviewing and Editing. Sergio Paulo Dejato Rocha: Project administration, Supervision, Writing- Original draft preparation, Writing- Reviewing and Editing.

Funding

The Article Processing Charge (APC) for the publication of this research was funded by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) (ROR identifier: 00x0ma614). This work was supported by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - [Finance Code 001]; and the National Council for Scientific and Technological Development CNPq (409335/2021-5 Chamada CNPq/MCTI/FNDCT Nº 18/2021—Faixa B—Grupos Consolidados and 305972/2022-7 to RK.

Data Availability

The datasets generated during and/or analyzed during the current study are available in the NCBI database under accession number: BioProject PRJNA1173088, and the plasmids as AP010962 and AP005147. Repository, https://www.ncbi.nlm.nih.gov.

Declarations

Conflict of interest

The authors declared that they have no conflict of interest that is relevant to the contents of this article.

Consent for Publication

Not applicable.

Consent to Participate

Not applicable.

Ethical Approval

This article does not contain any studies related to human participants or animals. Therefore, no ethical approval is involved.

Footnotes

Publisher’s Note

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

The datasets generated during and/or analyzed during the current study are available in the NCBI database under accession number: BioProject PRJNA1173088, and the plasmids as AP010962 and AP005147. Repository, https://www.ncbi.nlm.nih.gov.

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