https://orcid.org/0000-0001-5600-413X
Figures
Abstract
This study examines phenotypic antimicrobial resistance (AMR) and its genetic background in Escherichia coli isolated from poultry flocks in Türkiye, with a particular focus on extended spectrum β-lactamase (ESBL)-producing strains. A total of 918 E. coli isolates obtained from ceacal samples of chickens (n = 745) and turkeys (n = 173) were subjected to antimicrobial susceptibility testing using the agar disk diffusion method. Overall, high resistance rates were observed to tylosin (99.6%), ampicillin (90.8%), and oxytetracycline (84.0%), while resistance to third-generation cephalosporins (cefotaxime/ceftazidime) was detected in 11.4% of the isolates. Notably, AMR profiles varied significantly between poultry companies, indicating heterogeneous antimicrobial selection pressures within the production sector. ESBL-producing E. coli isolates exhibited high levels of multidrug-resistance, particularly to sulfamethoxazole (91.4%) and chloramphenicol (90.5%). Whole-genome sequencing (WGS) of ESBL-producing E. coli isolates (n = 87) identified several ESBL-encoding genes, with blaCTX-M-55 being the most prevalent (51.7%). Plasmid analysis demonstrated frequent associations of blaCTX-M-15 with IncFIB replicon, while blaCMY-2 was mainly linked to IncHI2A and IncI1-I plasmid types. In silico typing identified 44 distinct serotypes and 35 sequence types (STs), with O23:H4 and ST1011 being the most detected, highlighting the broad population structure of poultry associated E. coli. Virulence-associated genes were widely distributed among ESBL-producing isolates and predominantly related to adhesion, iron acquisition, stress response, and secretion systems. To the best of our knowledge, this study provides the first comprehensive WGS-based analysis of AMR in commensal E. coli from poultry in Türkiye, revealing significant public health concerns and the need for enhanced monitoring strategies.
Citation: Şahin S, Celil Özaslan BG, Moğulkoç MN, Karadağ M, Hammerl JA, Grobbel M, et al. (2026) Antimicrobial resistance profiles and whole-genome sequence analysis of extended-spectrum β-lactamase (ESBL) production in commensal Escherichia coli from poultry in Türkiye. PLoS One 21(4): e0344717. https://doi.org/10.1371/journal.pone.0344717
Editor: Grzegorz Woźniakowski, University of Nicolaus Copernicus in Torun, POLAND
Received: December 10, 2025; Accepted: February 24, 2026; Published: April 8, 2026
Copyright: © 2026 Şahin et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: The datasets generated and analyzed during the current study are publicly available in the National Center for Biotechnology Information (NCBI) repository under BioProject accession number PRJNA1168892. The data can be accessed at: https://www.ncbi.nlm.nih.gov/. The repository location and accession number are clearly stated to ensure full accessibility and reproducibility.
Funding: The author(s) received no specific funding for this work.
Competing interests: The authors have declared that no competing interests exist.
Introduction
Since the mid-20th century, antimicrobials have been widely used in animal production for therapeutic, prophylactic, and metaphylactic purposes [1,2]. Although antimicrobial utilization has been found to be beneficial for animal health and productivity, it has also accelerated the emergence and spread of antimicrobial resistant bacteria in livestock, thereby contributing to their presence in human populations [3]. The use of antibiotics as growth promoters in food-producing animals has been prohibited in EU countries and in Türkiye since 2006 [4,5] leading to a substantial reduction in veterinary antimicrobial sales. For instance, in the United Kingdom, the sales of veterinary antimicrobial agents decreased from 67.8 mg/PCU (Population Correction Unit) in 2010 to 25.7 mg/PCU in 2022 [5]. Similarly, the Turkish poultry industry has restricted the use of certain antibiotics beyond therapeutic purposes [6]. Several countries have established national surveillance programs to monitor antimicrobial use and resistance in food-producing animals, including DANMAP, MARAN, and NORM-VET [7]. In line with these efforts, Türkiye has also implemented a national antimicrobial resistance (AMR) action plan coordinated by the Ministry of Agriculture and Forestry [8]. Despite these efforts, antimicrobials continue to be widely used in livestock production, and global antimicrobial consumption in animals is projected to increase substaintiall to approximately ~143,481 tonnes by 2040 [2]. This continued use is closely associated with the persistence and dissemination of antibiotic-resistant pathogens. However, in recent years, a decrease in the resistance rates among bacteria from food-producing animals for many substances was notified in European countries, including extended spectrum β-lactamase (ESBL) producing bacteria [9,10].
Commensal bacteria, especially Escherichia coli, are commonly used as indicator microorganisms to monitor antibiotic resistance in animals and the environment [11]. Poultry production systems have been identified as important reservoirs of resistant E. coli, including resistance to critically important antimicrobials for human medicine [12]. Of particular concern is the increasing resistance to third-generation cephalosporins, which has prompted expanded monitoring of ESBL and AmpC β-lactamases-producing bacteria within a One Health framework [13]. The zoonotic potential of ESBL-producing E. coli and the frequent association of CTX-M enzymes with co-resistance to critically important antimicrobials pose a significant threat to human health by limiting treatment options [14,15]. Although recent surveillance reports from Europe indicate generally low resistance levels to third-generation cephalosporins in food-producing animals, ESBL-producing E. coli remain a priority concern [7,9].
Although several studies have reported the presence of ESBL-producing E. coli in poultry and retail chicken meat samples in Türkiye [16–18], comprehensive data on phenotypic antimicrobial resistance in commensal E. coli from poultry, particularly combined with in-depth genomic characterization, remain limited. Moreover, information on the population structure and genetic determinants of ESBL- and AmpC-producing E. coli from this source is scarce. It was hypothesized that antimicrobial resistance profiles of commensal E. coli differ among poultry farms and production companies in Türkiye, and that ESBL-producing isolates harbor diverse CTX-M subtypes and resistance genes, with potential plasmid-mediated dissemination. Accordingly, the aim of this study was to investigate phenotypic antimicrobial resistance patterns and to characterize the genetic background of ESBL-producing commensal E. coli isolated from poultry flocks in Türkiye using whole-genome sequencing (WGS).
Materials and methods
Composition of the study collection
Poultry caecal samples were collected in the framework of an ongoing research project on tigecycline-resistant Enterobacterales (TUBITAK, Project No: 121N855). Details of sampling are given in Kürekci et al. [19]. Shortly, ceacal samples (n = 940) were taken from healthy animals at slaughter, ten samples per flock from a total of 94 flocks which belonged to chicken companies (A, B and C) and one turkey company (D).
Samples were inoculated onto Eosin Methylene Blue agar (EMB Oxoid, CM0069B, Basingstoke, UK) and cultivated aerobically at 37 ºC for 24 hours. Presumptive E. coli colonies (one colony from each sample) were selected based on the appearance of a green metallic sheen and was transferred to Blood Agar Base to obtain a pure strain culture. Species identification of the isolates was performed using a Bruker Biotyper (MALDI-TOF MS, Bruker Daltonics GmbH & Co. KG, Bremen, Germany). Species confirmation was conducted by PCR targeting the uspA gene as described by Chen and Griffiths [20].
Antimicrobial susceptibility testing (AST) by agar disc diffusion
In this study, E. coli isolates were further investigated for their susceptibility to 16 antimicrobials/antimicrobial combinations comprising seven antibiotic classes used in human and/or veterinary medicine by using agar disk diffusion assay according to Clinical Laboratory Standard Institute standards [21]. Ciprofloxacin (CIP: 5 µg), enrofloxacin (ENR: 5 µg), florfenicol (FFC: 30 µg), chloramphenicol (CHL: 30 µg), tetracycline (TET: 30 µg), tigecycline (TGC: 15 µg), doxycycline (DO: 30 µg), oxytetracycline (T: 30 µg), trimethoprim-sulfamethoxazole (SXT: 25 µg), gentamycin (CN: 10 µg), amoxicillin/clavulanic acid (AMC: 30 µg), ampicillin (AMP: 10 µg), cefotaxime (FOT: 30 µg), ceftazidime (TAZ: 30 µg), imipenem (IPM: 10 µg), and tylosin (TYL: 15 µg) impregnated discs (Bioanalyse, Ankara, Türkiye) were used in this study. Escherichia coli strain ATCC 25922 was used as quality control strain. Isolates were classified as MDR when they exhibit resistance to three or more antimicrobials of distinct classes. According to CLSI [21], susceptibility categories were interpreted; however, intermediate (I) isolates were not evaluated as a distinct category. Instead, they were grouped with susceptible (S) isolates, and antimicrobial susceptibility outcomes were presented dichotomously as susceptible (S) or resistant (R).
Additional AST by broth microdilution for phenotypic dissection of ESBL-producing E. coli
For E. coli isolates, that were found to be resistant to TAZ and FOT by agar disc diffusion assay, minimum inhibitory concentrations (MIC) to 15 antimicrobials was further determined by broth microdilution following ISO 20776–1:2019 with commercial plates (SensititreTM EUVSEC3, Thermo Scientific, UK). The plate-layout included the following antimicrobial agents and ranges: AMP (1–32 mg/L), FOT (0.25–4 mg/L), TAZ (0.25–8 mg/L), meropenem (MERO) (0.03–16 mg/L), azithromycin (AZI) (2–64 mg/L), amikacin (AK) (4–128 mg/L), CIP (0.015–8 mg/L), nalidixic acid (NAL) (4–64 mg/L), CHL (8–64 mg/L), colistin (COL) (1–16 mg/L), CN (0.5–16 mg/L), TET 2–32 mg/L), TGC (0.25–8 mg/L), trimethoprim (TMP) (0.25–16 mg/L) and sulfamethoxazole (SMX) (8–512 mg/L). For quality controls, E. coli ATCC 25922 and a carbapenemase-producing Acinetobacter baumannii (BfR-AB-00019) were used. MIC results were interpreted according to the European Committee on Antimicrobial Susceptibility Testing (EUCAST) epidemiological cut-off values (http://www.eucast.org), as fixed in Commission Implementing Decision (EU) 2020/1729 (AK > 4 mg/L, AMP > 8 mg/L, FOT > 0.25 mg/L, TAZ > 0.5 mg/L, CHL > 16 mg/L, CIP > 0.06 mg/L, COL > 2 mg/L, CN > 2 mg/L, MERO > 0.125 mg/L, NAL > 8 mg/L, SMX > 64 mg/L, TET > 8 mg/L, TGC > 0.5 mg/L, TMP > 2 mg/L). Isolates were regarded as MDR when they exhibited resistance to three or more antimicrobials from distinct classes [22].
Whole-genome sequencing and bioinformatics analyses
One ESBL-producing E. coli per resistance profile and sample was subjected to short-read WGS on an Illumina NextSeq500 platform (Illumina, San Diego, CA, USA). Genomic DNA (gDNA) for Illumina sequencing libraries were extracted using the PureLink Genomic DNA Mini Kit (Invitrogen/ThermoFisher Scientific) as recommended by the manufacturer’s protocol. Purity and quality parameters of the gDNA were with the Qubit 4.0 Fluorometer according to the standard protocol. Short-read, paired-end sequencing runs were performed in 1x149 cycles on a NextSeq500 benchtop device using the Illumina NextSeq Mid Output Kit v2.5 (300 Cycles) (Illumina, San Diego, CA, USA). After trimming of the raw reads, the sequences were subjected to the AQUAMIS pipeline (https://gitlab.com/bfr_bioinformatics/AQUAMIS) [23]. de novo read assembling was performed using the SPAdes (version 3.14.1) of the Bacterial and Viral Bioinformatics Resource Center (BV-BRC) (https://www.bv-brc.org/) [24]. Final annotation of the bacterial genomes was conducted using the automated submission portal (https://submit.ncbi.nlm.nih.gov/) of the National Center for Biotechnology Information (NCBI) under bioproject No PRJNA1168892.
Further in silico-typing purposes (i.e., MLST, cgMLST and serotype prediction) as well as the detection of resistance/virulence genes and plasmids was conducted by using the BakCharak pipeline v3.1.6 (https://gitlab.com/bfr_bioinformatics/BakCharak), including plasmidfinder (db version 2022-07-13) and mlst v2.23.0 with pubmlst database (version 2025-02-27). cgMLST was performed using chewieSnake pipeline (https://gitlab.com/bfr_bioinformatics/chewieSnake). The minimum spanning tree is distance based and was visualized by iTOLv7 using cgMLST profile data (2,513 loci).
Statistical analysis and visualization
The chi-square test was used to compare the proportions of antimicrobial resistance among companies, with a p-value of <0.05 considered statistically significant. The Multiple Antibiotic Resistance Index (MAR) index for ESBL-producing E. coli was calculated and interpreted according to Krumperman [25] using the formula: a/b, where ‘a’ represents the number of antibiotics to which an isolate was resistant, and ‘b’ represents the total number of antibiotics tested. Indices are larger than 0.2 if an isolate originates from a source where antibiotics are used to a great degree and/or in large amounts [26]. Percentage changes in antimicrobial resistance (AMR) rates were calculated using poultry company A as the reference group. The percentage change was determined through the following formula: .
Results
Apart from high resistance levels to tylosin, ampicillin and oxytetracycline, the commensal E. coli from the four companies exhibit distinct differences in their AMR profiles
A total of 918 E. coli (company distribution; A: n = 279, B: n = 236, C: n = 230 and D: n = 173) were obtained from chicken and turkey ceacal samples. AST results from disc diffusion assay is given in Table 1. AMR rates varied significantly among poultry companies (Fig 1), with the highest resistance levels observed for TYL (98.3–100.0%), AMP (86.9–99.6%), T (78.6–87.7%), TET (67.0–80.6%), FFL (40.5–81.8%) and SXT (41.0–64.8%), while DO resistance was moderate in chicken companies (13.9–19.5%). In total, 11.4% and 1.5% of the strains exhibited resistances to FOT/TAZ and TGC, respectively. Resistances against imipenem could not be detected among the isolates. In terms of the antibiotic resistance profiles, significant statistical differences were found for CIP, ENR, FFC, CHL, TET, SXT, CN, AMC, AMP, FOT, and TAZ between companies A, B, C, and D (p < 0.001; p.001), as summarized in Table 1. Resistance to CN was significantly higher in samples from the three chicken companies compared to those of the turkey company (11.3–22.9% versus 9.8%; p < 0.001). Regarding the aminopenicillins, resistance to AMC was low in companies A, B, and D (17.9%, 16.9% and 3.5%, respectively), compared to the very high level in chicken company C (90.9%) (Table 1; Fig 1). Among the 3rd generation cephalosporins, resistance to FOT/TAZ was determined to be 7.6–20.4% in chicken companies (A-C) and 4.0% in the turkey company (D).
A, B, C (chicken companies) and D (turkey company) are representing individual companies. Ciprofloxacin (CIP), enrofloxacin (ENR), florfenicol (FFC), chloramphenicol (CHL), tetracycline (TET), tigecycline (TGC), doxycycline (DO), oxytetracycline (T), trimethoprim-sulfamethoxazole (SXT), gentamycin (CN), amoxicillin/clavulanic acid (AMC), ampicillin (AMP), tylosin (TYL), imipenem (IPM), cefotaxime (FOT) and ceftazidime (TAZ).
Table 2 displays the percentage changes in antimicrobial resistance rates of poultry companies B, C, and D relative to company A. The most striking finding was the markedly higher resistance in company C to amoxicillin/clavulanic acid (+407.8%) and third-generation cephalosporins (+72.9%). In contrast, company D generally exhibited lower resistance levels across most antimicrobial classes, while complete or near-complete decrease in tigecycline resistance were observed in all companies relative to company A.
Apart from ESBL-production, high level of MDR was determined for poultry E. coli
Of the 918 E. coli isolates, a total of 105 E. coli displayed phenotypic resistance to 3rd generation cephalosporins in agar disc diffusion assays and are thus assigned as presumptive ESBL-producers and further subjected to broth microdilution testing for MIC determination.
The majority of them revealed MDR patterns, being resistant to antibiotics of more than three classes. As expected, all of these isolates were resistant to AMP (100%), FOT (100%) and TAZ (100%). Further the highest resistance rates were detected for SMX (91.4%; n = 96/105), (CHL (90.5%; n = 95/105), TET (87.6%; n = 92/105), CIP (83.8%; n = 88/105) and NAL (75.2%; n = 79/105). The resistance rate for CN and AZI were (34.3%; n = 36/105) and (21.9%; n = 23/105), respectively. It is also noteworthy that resistance against MERO (1%; n = 1) and COL (1%; n = 1) was detected. However, none of the isolates were found to be resistant to AK or TGC (Table 3). The MAR index of ESBL-producing E. coli was found to be SMX 0.91, CHL 0.90, TET 0.87, CIP 0.83, NAL 0.75, TMP 0.67, GEN 0.34, AZI 0.21, MERO 0.01 and COL 0.01.
CTX-M is the most prevalent enzyme conferring ESBL status within the genetically highly diverse E. coli collection
In this study, 99 ESBL-producing E. coli strains were selected for WGS. Based on the SNP analysis, only one clone per flock was selected for further in-depth analyses, leaving 87 ESBL-conferring E. coli genomes. WGS provided detailed insights about individual genetic determinants responsible for the observed phenotypic resistances and indicate the broad diversity of the occurring E. coli populations in chicken and turkey. Among the genomes, five different blaCTX-M genes were identified. The most abundant are blaCTX-M-55 accounting for 51.7% (n = 45/87) of the isolates, followed by blaCTX-M-15 (18.4%; n = 16/87), blaCTX-M-1 (3.4%; n = 3/87), blaCTX-M-27 (1.1%; n = 1/87), and blaCTX-M-8 (1.1%, n = 1/87) (Table 4). Additionally, AmpC β-lactamase genes blaCMY-2 23.0% (n = 20/87) and blaDHA-1 were found in 2.3% (n = 2/87) of the isolates. In addition, also non-ESBL blaTEM gene variants like blaTEM-1A, blaTEM-1B, blaTEM-1C and blaTEM-176 were found in 62.1% (n = 54/87) of the isolates, while blaOXA-1 and blaOXA-4 occur in 1.1% (n = 1/87) and 10.7% (n = 3/87) of the isolates, respectively.
Overall, 44 different serotypes were identified in-silico among the 87 ESBL-producing E. coli. Both O and H antigens were predicted for 94.3% (n = 82) of the strains, however the O antigens of five genomes (5.68%) were not typeable. The most common detected serotypes were O23:H4 (6.8%, n = 6/87), followed by O83:H42 (5.7%, n = 5/87) and O9:H12, O18:H49, O100:H30, O102:H9, O136:H26, and O160:H4 (3.4%, n = 3/87). Other commonly recorded serotypes are given in S1 Table.
Commensal E. coli from poultry exhibit a broad set of AMR determinants
Different proportions of strains harbored genes encoding for resistance to tetracycline’s [tet(A) (n = 76) and tet(B) (n = 8)], quinolone [qnrS1 (n = 6); qnrB4 (n = 2); qnrB19 (n = 8) and aac(6‘)-Ib-cr (n = 1)], folate pathway inhibitors [(dfrA1 (n = 53), dfrA5 (n = 5), dfrA12 (n = 10), dfrA14 (n = 15), dfrA17 (n = 23) and dfrA36 (n = 1)], sulfonamide [sul1 (n = 13), sul2 (n = 54) and sul3 (n = 37)], macrolides [mph(A) (n = 18), mph(B) (n = 1), erm(42) (n = 1) and erm(B) (n = 1)], lincosamides [lnu(F) (n = 25) and lnu(G) (n = 1)], phenicols [catA1 (n = 8), catB2 (n = 4), cmlA1 (n = 33), catB3 (n = 4) and floR (n = 73)], aminoglycosides [aac(3)-IId (n = 23), aac(3)-IIe (n = 6), aadA1 (n = 43), aadA2 (n = 36), aadA5 (n = 21), aadA22 (n = 1), ant(2’‘)-Ia (n = 4), aph(3’)-Ia (n = 38), aph(3’‘)-Ib (n = 54), aph(3’)-XV (n = 3), aph(4)-Ia (n = 1), aph(6)-Id (n = 54) and aac(6‘)-Ib-cr (n = 1)]. Furthermore, we detected the mcr-1 gene in one colistin-resistant strain from a chicken caecum sample (S1 Table).
A high genetic diversity was determined in the representative commensal E. coli study strain collection
The majority of the 87 ESBL-producing E. coli were assigned to phylogenetic groups B1 (27.6%, n = 24), A (25.3%, n = 22) and D (24.1%, n = 21). Phylogenetic group F (13.8%, n = 12), representing a novel group D related cluster, was less prevalent. Seven isolates (8.0%) were assigned to phylogenetic group E and one isolate (1.1%) belonged to group G. Phylogroups B2, frequently harboring more pathogenic E. coli, and group C were not detected in this study.
Multi Locus Sequence Typing following the Achtmann scheme assigned 85 of the isolates to 35 different sequence types (STs), while the allele profile of two strains (BfR-23-MO00238, BfR-23-MO00269) does not match to a designated ST of the pubMLST database. There are 20 STs, which are represented by more than one isolate, with ST1011 being the most prevalent (n = 8) detected in isolates from the chicken companies A, B and C. The other ST types were ST10 (n = 6), ST1882 (n = 6), ST58 (n = 5), ST1485 (n = 5), ST93 (n = 4), ST162 (n = 4), ST38 (n = 4), ST155 (n = 3), ST189 (n = 3), ST212 (n = 3), ST746 (n = 3), ST4274 (n = 2), ST624 (n = 2), ST101 (n = 2), ST219 (n = 2), ST770 (n = 2), ST6027 (n = 2), ST648 (n = 2), and ST744 (n = 2). The remaining 15 isolates represented individual STs (ST57, ST69, ST117, ST156, ST295, ST354, ST457, ST665, ST752, ST1431, ST1723, ST3941, ST4373, ST7941 and ST10343).
Phylogenetic SNP analysis
A phylogenetic tree was inferred from the cgMLST results of all 87 E. coli strains (Fig 2). A distance threshold of 10 revealed 69 distinct clusters, highlighting the high genetic diversity within the tested E. coli population. The largest cluster consisted of four E. coli isolates from four different farms, all belonging to company B. Beyond these clonal clusters, isolates originating from different regions and farms were interspersed throughout the phylogenetic tree, suggesting that genetically diverse ESBL-producing E. coli strains are widely distributed across poultry production areas in western Türkiye.
The isolate IDs are shown around the circular illustration. From the outside to the inside the four circles show the poultry companies (A, B, C and D), the animal species of the sample (chicken and turkey), the detected CTX-M genes and the Clermont types (phylogenetic group) they belong to, differentiated by color codes as given in the legend.
Escherichia coli genomes exhibit a broad set of plasmid types of which especially IncHI2A and IncFIB carry ESBL and AmpC determinants
PlasmidFinder was used to predict at least one plasmid replicon type in each of the ESBL-producing E. coli (S1 Table). The most frequent replicon sequences were: IncFIB (AP001918) (n = 60), Col (MG828) (n = 42), ColRNAI (n = 40), IncFIC (FII) (n = 39), Col440I (n = 22), IncI1 (Alpha) (n = 19), pKPC-CAV1321 (n = 18), p0111 (n = 18), IncHI2A (n = 18), IncFIA (n = 16), Col156 (n = 14) and IncFIB(pHCM2) (n = 10). The other less frequently found replicon types are IncX1 (n = 7), ColpVC (n = 6), IncB/O/K/Z (n = 6), IncX4 (n = 5), IncFII (pCoo) (n = 5), Col8282 (n = 5), IncQ1 (n = 4), IncY (n = 4), IncI2 (Delta) (n = 4), IncHI2 (n = 4), IncFII (29) (n = 3), pUTI89 (n = 3), Col(MP18) (n = 2), IncX3 (n = 1), IncN (n = 1), BS512 (n = 1), ColE10 (n = 1), IncFIB (pB171) (n = 1), IncFII (pRSB107) (n = 1), IncFII (pSE11) (n = 1) and IncFIA (HI1) (n = 1).
In 26 of the isolates the contig harboring the ESBL or AmpC gene also harbored plasmid markers. In five isolates blaCTX-M-15 was associated with IncFIB type plasmid, in one with an p0111. Two isolates harbored blaCTX-M-1 genes associated with a IncI1 plasmid, another isolate a blaCTX-M-55 with an IncFIC plasmid. blaCMY-2 was frequently associated with plasmids. In nine isolates it was found together with IncHI2A, in eight isolates with an IncI1 and in two isolates with and IncB plasmids.
Virulence genes
In this study, numerous virulence-associated genes (VAGs) have been detected in the genomes of ESBL-producing E. coli. Using the WGS data, VAGs were selected from public databases included in the E. coli functional genotyping. We identified 58–124 VAGs in all ESBL-producing E. coli strains using WGS. In-silico, the genomes were screened for the presence of adherence, antimicrobial activity/competitive advantage, effector delivery system, immune modulation, invasion, nutritional/metabolic factor and regulation groups of virulence. In this collection, the most uniformly conserved virulence factors, detected in 100% of the strains, were ompA, ibeC, entA-E, fepB, phoP, rpoS, rcsB, fur, and tssA/tssM. These highly conserved genes are mainly related to adhesion, iron acquisition, stress response, and secretion systems, indicating a strong adaptive potential of the isolates.
Discussion
Since 2014, member states of the European Union (EU) have been using E. coli as a common commensal indicator bacterium for monitoring AMR in farm animals [7]. To the best of our knowledge, there is no comparable regulatory framework implemented in Türkiye. Therefore, this preliminary study was carried out to establish a baseline data for the future investigations.
Studies including E. coli isolates from poultry and other farm animals, both commensal and pathogenic, have demonstrated resistance to multiple antibiotics, including TET, NAL, SMX, TYL, PEN and AMP [14,27]. Although there are a number of existing local reports, in which isolates were collected without uniformed isolation criteria, and such inconsistency makes the comparison difficult. Despite these limitations, the resistance patterns observed in the present study are largely comparable to those reported from poultry production system in Europe and other regions [10,12,28]. Our findings show a clear host-associated divergence in resistance patterns, as CIP, AMC, FFC, CHL and SXT resistance was found to be significantly higher among E. coli isolates from chickens, when compared to those obtained from turkey. On the other hand, doxycycline resistance was remarkably higher among E. coli isolates from turkey farm than those obtained from chicken farms. This difference could be attributed to comparatively limited antibiotic usage in turkey production, nonetheless, only farms of one turkey producer was included, representing a limitation for this study.
Our study found a very high rate of resistance to TYL, AMP, and T among commensal E. coli from poultry samples in Türkiye. These findings closely mirror results from both national and international poultry studies, in which resistance to older and commonly used antimicrobials remains widespread [10,14,28,29]. High resistance rates to AMP, SMX, CIP, and NAL have been consistently reported in both national studies, European Union surveillance reports, and large scale meta analyses across Europe and globally [9,12,29]. On the other hand, lower AMP resistance levels among E. coli from chickens and fattening turkeys in the European report was also reported to be 46.6% and 55.8%, respectively [9]. Additionally, significant resistance to CIP (48.4%), a critically important antimicrobial, was observed in the current study, reflecting concerns about widespread resistance to quinolone antibiotics in poultry [30]. In contrast, a recent study from Australia reported a markedly low CIP resistance rate (3.3%) among poultry-associated E. coli, which has been attributed to the long-standing restriction of quinolone use in poultry production and as well as resitrictions on the importation of live poultry and fresh meat [11]. This comparison highlights the strong association between national antimicrobial usage policies and the emergence of fluoroquinolone resistance in poultry-associated E. coli.
In our study, resistance to cefotaxime and/or ceftazidime differed by poultry company and species, remaining low in fattening turkeys (4.0%) and chickens from companies A and B (7.6%−11.8%), while reaching higher levels in chickens from company C (20.4%). Notably, a recent large-scale Australian study analyzing E. coli isolates from approximately 2,950 meat chickens reported no resistance to FOT or TAZ [11]. Differences likely reflect variations in antimicrobial usage practices among companies. In addition, 11.4% of the E. coli isolates recovered from poultry caecal samples (98 chickens and seven fattening turkeys) were identified as ESBL-producing strains (n = 105/918). This proportion reflects the frequency among recovered isolates, not the prevalence at sample level, as selective screening for ESBL-producing E. coli was not performed on all caecal samples. According to EFSA/ECDC [31], the proportion of ESBL-producing E. coli strains in chickens across EU member states ranges from 0.6% to 7.1%, while values in fattening turkey range between 0.6% and 6.3%. Similarly low strain-based frequencies have been reported in Asian countries, including Malaysia (5.5%) [32] and South Korea (7.0%) [33]. However, higher strain-based frequencies have also been reported in Hungary (34.2%) [34] and Italy (43.6%) [35], as well as in African settings, such as Ghana (29.0%) [36]. Similarly, ESBL producing E. coli frequencies in turkeys vary internationally, ranging from 2.2% in Portugal [37] to 5.0% in Canada [38] and 6.8% in Egypt [39].
WGS analysis demonstrated a broad genetic diversity of β-lactamase determinants within the E. coli population, including blaCTX-M, blaTEM, blaOXA, and blaCMY-2 variants, which is consistent with previous reports [13]. In our study, the predominant ESBL genes were blaCTX-M-55 and blaCTX-M-15, while blaCMY-2 and blaDHA-1 were the main AmpC genes identified. While comparative data from other countries show that blaCTX-M-1 can occur at much higher rates, such as in poultry feces and farm environments in Germany (41%) [40] and chicken isolates in Canada (91%) [41], the proportion of blaCTX-M-1 detected in our study was notably lower. Several earlier studies have also reported that other β-lactamase genes, including blaSHV and blaCMY-2, may be more prevalent than blaCTX-M variants [42–44]. Such variability has been attributed to factors such as antimicrobial usage patterns, environmental and geographical characteristics, and plasmid mobility [45].
A notable trend observed globally is the shift from blaCTX-M-15 to blaCTX-M-55 in poultry-associated E. coli. While blaCTX-M-15 had previously been dominant in countries such as Germany and various African countries [36,46], Türkiye was among the first to report a rapid increase in blaCTX-M-55 prevalence [16,17]. Similar transitions have been documented in other regions, including China [47–49]. Consistent with these observations, Dugget et al. [49] reported that while blaCTX-M-1 was the most common ESBL gene in poultry isolates from 2016−2018, by 2020 the dominant variant had shifted to blaCTX-M-55. Additionally, ESBL-producing E. coli from chickens have been shown to transfer β-lactam resistance via extracellular vesicle (EV)-mediated horizontal gene transfer, providing a plausible mechanism for the rapid dissemination of these genes. Recent evidence also suggests that ESBL-producing E. coli may disseminate blaCTX-M-55 through EV-mediated horizontal gene transfer. Xu et al. [50] reported that EV-mediated transfer of blaCTX-M-55 is not random; rather, it appears to be selective and may occur more efficiently between closely related bacterial species. Additionally, the detection of CTX-M-55 across multiple plasmid backbones in livestock-associated E. coli raises concern that the gene is becoming increasingly mobile, thereby enhancing its capacity for rapid spread within and between bacterial populations. Given this mobility, routine genetic monitoring of CTX-M variants is essential for detecting emerging mutations and tracking the dissemination pathways of ESBL genes. Strengthening surveillance systems and developing targeted control strategies are therefore critical to limit the further expansion of blaCTX-M-55 within both animal and human reservoirs.
Phenotypic resistance patterns showed good agreement with resistance determinants detected by WGS using ResFinder. Among these findings, colistin resistance was detected in a single isolate, which was confirmed by the presence of the plasmid-mediated mcr-1 gene. This observation is in line with previous studies reporting a low prevalence of mcr-1 among retail poultry meat in Türkiye [18,51]. Although mcr-1 remains infrequently detected, its occurrence in the poultry production chain highlights the importance of continued surveillance due to its potential for horizontal dissemination.
In our study, ESBL-producing E. coli strains exhibited a diverse range of phylogroups, with B1 being the most common (27.6%), followed by A (25.3%), D (24.1%), and F (13.8%). Also, phylogroup E and G were detected in low proportions. Notably, one isolate was identified as belonging to the G phylogroup, an intermediary between F and B2. These findings align with previous studies, which indicate that phylogroups A and B1 are typically commensal, while B2, D and E are often pathogenic; the presence of D phylogroup isolates suggests potential for commensal strains to become pathogenic under certain conditions [13].
The high number of STs, together with the wide SNP variation observed in the isolates, suggests multiple contamination sources rather than clonal expansion, a pattern similarly described in the poultry production chain. Despite this diversity, ST1011 and ST10 were the most frequent STs. Notably, six of the top 20 ExPEC-associated lineages were detected (ST10, ST38, ST58, ST69, ST117, ST354), all of which are well-recognized contributors to both human and animal infections [52]. ST10 is widely reported as a dominant MDR lineage in animals [53]. Notably, a single ST69 isolate carried blaCMY-2, a lineage previously described as globally disseminated in poultry [54].
In this study, ESBL-producing E. coli isolates carried a broad set of VAGs, including adhesion factors (e.g., fim, papC and sfa), enterotoxin genes (est), the intimin gene (eae), and iron acquisition systems such as iutA, fyuA, and iucC. The presence of these genes aligns with previously reported virulence profiles of avian ExPEC-related lineages [13]. While the detection of these VAGs indicates that some isolates possess traits associated with extra-intestinal pathogenicity, our data do not allow conclusions regarding zoonotic transmission. Instead, these findings highlight the need for continuous surveillance to monitor the co-occurrence of virulence and resistance determinants in poultry-associated E. coli populations.
Plasmids play a crucial role in the worldwide spread of ESBL genes [12]. Previous studies have identified variable plasmid replicon types including IncFIB, Col(MG828), IncFII, IncFIC(FII) and IncX1 [33,55]. In the current study, IncFIB, Col(MG828) and ColRNAI were the most frequent replicon types encountered in ESBL producing E. coli, followed by IncFIC(FII), Col440I and IncI1 (Alpha). In South Korea, blaCTX-M-55 positive E. coli isolates have also been reported to carry IncF plasmids in combination with other replicon types such as FIB, I1-Ig, K, N, and/or FIA [33]. Overall, these findings indicate that IncF and Col-type plasmids constitute common and well-adapted genetic backbones in poultry-associated E. coli populations across different regions, facilitating the maintenance and dissemination of ESBL determinants within poultry production systems.
Conclusion
In this study, high resistance to TYL, AMP, T, TET, FFL, and SXT was found among commensal E. coli isolates from poultry, with marked differences in resistance prevalence between poultry companies. WGS analysis provided detailed insights into the genetic characteristics of these strains, revealing diverse MLST profiles, with ST1011 identified as the most frequent sequence type. Among ESBL producing isolates, the blaCTX-M-55 gene emerged as the most common ESBL determinant, frequently associated with transferable plasmid replicon types, indicating a high potential for dissemination within the poultry production chain. Although the study was limited by the lack of detailed farm-level antimicrobial usage data, these findings provide valuable baseline information for Türkiye and highlights the need for continuous, harmonized AMR surveillance and targeted control strategies in the poultry sector.
Supporting information
S1 Table. WGS data of ESBL-producing Escherichia coli isolates.
https://doi.org/10.1371/journal.pone.0344717.s001
(XLSX)
Acknowledgments
Seyda Şahin is a recipient of a Werner Baltes fellowship at the German Federal Institute for Risk Assessment (BfR), Berlin, Germany. The authors are grateful to The Scientific and Technological Research Council of Türkiye (TUBITAK) for postgraduate scholarship to Büşra Gülay Celil Özaslan (Project No: 121N855).
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