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Article

Genome-Wide Analysis of Escherichia coli Isolated from Dairy Animals Identifies Virulence Factors and Genes Enriched in Multidrug-Resistant Strains

by
Bradd J. Haley
1,*,
Seon Woo Kim
1,
Serajus Salaheen
1,
Ernest Hovingh
2 and
Jo Ann S. Van Kessel
1
1
Environmental Microbial and Food Safety Laboratory, Beltsville Agricultural Research Center, Agricultural Research Service, United States Department of Agriculture, 307 Center Drive, Beltsville, MD 20705, USA
2
Department of Veterinary and Biomedical Sciences, Pennsylvania State University, University Park, PA 16802, USA
*
Author to whom correspondence should be addressed.
Antibiotics 2023, 12(10), 1559; https://doi.org/10.3390/antibiotics12101559
Submission received: 23 September 2023 / Revised: 16 October 2023 / Accepted: 16 October 2023 / Published: 23 October 2023
(This article belongs to the Section Mechanism and Evolution of Antibiotic Resistance)
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Abstract

:
The gastrointestinal tracts of dairy calves and cows are reservoirs of antimicrobial-resistant bacteria (ARB), which are present regardless of previous antimicrobial therapy. Young calves harbor a greater abundance of resistant bacteria than older cows, but the factors driving this high abundance are unknown. Here, we aimed to fully characterize the genomes of multidrug-resistant (MDR) and antimicrobial-susceptible Escherichia coli strains isolated from pre-weaned calves, post-weaned calves, dry cows, and lactating cows and to identify the accessory genes that are associated with the MDR genotype to discover genetic targets that can be exploited to mitigate antimicrobial resistance in dairy farms. Results indicated that both susceptible and resistant E. coli isolates recovered from animals on commercial dairy operations were highly diverse and encoded a large pool of virulence factors. In total, 838 transferrable antimicrobial resistance genes (ARGs) were detected, with genes conferring resistance to aminoglycosides being the most common. Multiple sequence types (STs) associated with mild to severe human gastrointestinal and extraintestinal infections were identified. A Fisher’s Exact Test identified 619 genes (ARGs and non-ARGs) that were significantly enriched in MDR isolates and 147 genes that were significantly enriched in susceptible isolates. Significantly enriched genes in MDR isolates included the iron scavenging aerobactin synthesis and receptor genes (iucABCD-iutA) and the sitABCD system, as well as the P fimbriae pap genes, myo-inositol catabolism (iolABCDEG-iatA), and ascorbate transport genes (ulaABC). The results of this study demonstrate a highly diverse population of E. coli in commercial dairy operations, some of which encode virulence genes responsible for severe human infections and resistance to antibiotics of human health significance. Further, the enriched accessory genes in MDR isolates (aerobactin, sit, P fimbriae, and myo-inositol catabolism and ascorbate transport genes) represent potential targets for reducing colonization of antimicrobial-resistant bacteria in the calf gut.

1. Introduction

Multidrug-resistant (MDR) Escherichia coli are frequently isolated from dairy cow and calf feces, unpasteurized cow’s milk, and culled dairy cow beef and are a major component of the suite of antimicrobial-resistant bacteria (ARB) carried by young calves [1,2,3]. A minority of these E. coli are enterohemorrhagic (EHEC) Shiga toxin-encoding strains that can cause moderate to severe gastrointestinal disease, septicemia, hemolytic uremia syndrome (HUS), chronic sequelae, and possibly death [4,5]. However, E. coli is highly diverse, with many suites of virulence and fitness factors (VFFs) that can cause both mild to severe gastrointestinal and extra-intestinal infections, such as urinary tract infections (UTIs) and meningitis [6]. Major non-EHEC strains causing human disease are typically classified into pathovars (pathotypes) based on the presence of different suites of virulence factors; strains that contain overlapping pathovar suites of these genes are considered hybrid pathovars. Dairy animals are known reservoirs of these MDR or antimicrobial-susceptible pathogens, but most studies of E. coli from these animals have either targeted only a few farms, have focused on a specific resistance phenotype/profile or pathovar, or have not utilized a genome-wide scale approach to evaluate the diversity and dynamics of these organisms in the dairy farm environment.
Dairy cow and calf feces are known reservoirs of ARGs that can contaminate milk, meat, other animals, animal handlers, and the environment [7,8]. Most studies using sensitive molecular techniques have shown that most, if not all, dairy animals carry antimicrobial-resistant bacteria (ARB) in their lower gastrointestinal system and feces, and this is consistent even in the absence of antimicrobial therapy [9,10,11,12]. Multiple studies have demonstrated that antimicrobial administration results in a transient or no increase in antimicrobial resistance (AMR) in the feces and that animals that were never exposed to these drugs may, at times, have the same level of resistance as conventionally raised animals [13,14,15]. Further, it has been repeatedly demonstrated that young calves typically carry a higher level of resistance than older lactating or dry cows, and this, too, is true in the absence of antimicrobial administration [1,2,8,16,17]. However, these calves are exposed to their dam’s microbial communities during and immediately after birth, as well as the surrounding birthing pen environment, all of which have a lower ratio of resistant to susceptible bacteria than that found in calf feces. The dam, the farm environment, colostrum, and milk/milk replacer are the sources of these ARBs, but not much is known about the genetic factors of these bacteria that influence their enrichment and persistence in the calf gut. This information could be used to potentially identify intervention targets to reduce the carriage of ARBs in dairy animals and possibly other food animals. Here, we used a genome-wide approach to evaluate the AMR profiles and virulence factor diversity of E. coli collected from pre-weaned calves, post-weaned calves, dry cows, and lactating cows on 80 commercial dairy farms. We also identify non-resistance conferring genes that co-occur with the MDR phenotype with the objective of identifying potential intervention targets to reduce the occurrence of MDR E. coli in dairy calves.

2. Materials and Methods

E. coli isolates were selected from a previously published study of antimicrobial resistance in bacteria isolated from the feces of animals in different age groups on 80 commercial dairy farms [1]. Selection was based on farm, animal group, and antibiotic sensitivity. Isolates were provisionally prescreened for antibiotic sensitivity by patch-plating onto eight petri dishes, each supplemented with a different class of antibiotics. Based on these data, one isolate per resistance group (MDR or susceptible), per animal group (pre-weaned calves, post-weaned calves, lactating cows, and dry cows), and per farm was identified. This resulted in eight groups of isolates (susceptible dry cow isolates = 315; MDR dry cow isolates = 52; susceptible lactating cow isolates = 1033; MDR lactating cow isolates = 136; susceptible post-weaned calf isolates = 221; MDR post-weaned calf isolates = 140; susceptible pre-weaned calf isolates = 132; MDR pre-weaned calf isolates = 284). Within each of these groups, random numbers were assigned to each isolate using a non-redundant random number generator in Microsoft Excel v. 16.77.1 (Microsoft Corporation, Redmond, WA, USA), and these numbers were reordered from smallest to largest, and the smallest number for each animal group within each farm was selected for genome sequencing.
Selected isolates were grown overnight at 37 °C in L broth (per 1 L: enzymatic digest of casein 10 g, yeast extract 5 g, sodium chloride 5 g), and DNA was extracted from these overnight cultures using a QiaCube platform (Qiagen, Hilden, Germany). Genome sequencing libraries were constructed using a Nextera XT kit (Illumina, La Jolla, CA, USA), and 2 × 150 bp paired-end sequencing was conducted on a NextSeq 500 platform (Illumina) with a High Output flow cell. After demultiplexing the data, reads were trimmed of adaptors, sequencing contaminants, and phiX sequences using DeconSeq [18] and then trimmed for quality and length using Trimmomatic (LEADING:20 TRAILING:20 SLIDINGWINDOW:4:20 MINLEN:36) [19]. These cleaned and curated reads were assembled using SPAdes V. 3.14.1 [20]. The genome sequencing data have been deposited at NCBI (Supplementary File S4).
Core genome SNPs were identified by aligning the 264 E. coli genomes used in this study with 118 publicly available Escherichia genomes representing the major phylogenetic groups (A, B1, B2, C, D, E, F, and G) and the near neighbors, E. fergussoni and E. albertii, downloaded from NCBI using the Harvest package [21]. ParSNP was run with the parameters -c and -x and the complete chromosome of E. coli K-12 substrate MG1655 (NCBI accession: NC_000913.3) as the reference genome (-r). Identified SNPs were used to infer a maximum likelihood tree with 1000 bootstrap replicates under default settings using RAxML [22].
Genome sequences were interrogated for transferrable ARGs, as well as SNPs, conferring resistance to antibiotics using the ResFinder 4.1 database with default settings (threshold for %ID = 90%, minimum length = 60%) [23]. Since our aim was to focus on ARGs, an isolate that was provisionally categorized as phenotypically susceptible but was found to carry an ARG (or ARGs associated with resistance to less than three classes of antimicrobials) was reclassified as “resistant” (R) and replaced with a phenotypically susceptible isolate from the same animal group and farm. This substituted isolate was then genomically confirmed as ARG-free. The same approach was taken to genomically validate the presence of ARGs and SNPs conferring resistance to three or more classes of antibiotics in provisionally phenotypical MDR isolates. A genome that encoded ARGs or SNPs conferring resistance to one or two classes of antibiotics was classified as “resistant” (R) and was included in that group for some downstream analyses. The final number of genome sequences used for this study was 108 multidrug-resistant (MDR), 36 antimicrobial-resistant (R), and 120 antimicrobial-susceptible (S) sequences.
Genotypic MDR genomes were identified as those genomes that encoded genes and SNPs known to confer resistance to at least three classes of antibiotics (identified as “MDR” in the analysis). Genotypic antibiotic-resistant isolates were those encoding genes or SNPs known to confer resistance to one or two classes of antibiotics (identified as “R”). Genotypic susceptible genomes were those that did not encode any known genes or SNPs that confer resistance to any antibiotics (identified as “S”). Isolates were not initially selected for sequencing based on resistance profile but were selected based on whether they were provisionally resistant to three or more antibiotics or no antibiotics, and, thus, the ARG content reflects an unbiased selection of MDR isolates. Sequence types (STs) and plasmid replicons were identified using MLST 2.0 [24,25] and PlasmidFinder 2.1 [26] with default settings. For genomes that did not match an exact ST in the MLST 2.0, the raw reads were uploaded to the Enterobase database for novel ST assignment [27].
Since virulence genes are numerous, highly diverse, and do not exclusively function to cause an infection within a mammalian host but also at times aid in survival within and outside of the host, we labeled these genes and the known major virulence factors collectively as “virulence and fitness factors” (VFF). VFFs were identified with ABRicate under default settings [28].
Identification of the pangenome was conducted by annotating the assembled genomes in PROKKA [29] under default settings and then uploading the gff3 files into Roary [30] under default settings. Using this pangenome, genes that were enriched (significantly more abundant) in MDR, as well as susceptible genomes, were identified using a Fisher’s Exact Test with the package “exact2 × 2” in R. To limit the proportion of falsely significant results, q-values (FDR—False Discovery Rate) [31] were estimated for all genes using the package “qvalue” in R (q-values are the proportion of genes that are identified as significant that are estimated to be falsely significant). A q-value threshold of <0.05 was used to identify significant features. Signal proteins were identified among the translated enriched genes to identify secreted proteins using SignalP 5.0 [32].
To visualize the distances between the accessory gene content (present in <99% of genomes) of MDR and susceptible genomes, a non-metric multidimensional scaling (NMDS) analysis using the Jaccard distance metric was inferred, followed by an analysis of similarities (ANOSIM) of the pangenomes of these two groups with and without ARGs included in the analyses using the R package “vegan”. To determine if MDR or S genomes were randomly distributed among the phylogenetic groups, a χ2 test was conducted in R.

3. Results

3.1. Antimicrobial Resistance Genes

In total, there were 838 ARGs detected, 46 of which were unique genes. Genomes encoded genes conferring resistance to between 0 and 8 classes of antibiotics (Table 1). The median and average number of classes to which MDR isolates were resistant were 5 and 4.6, respectively. Isolate genomes encoded between 0 and 16 ARGs, including resistance-conferring SNPs. Among the MDR isolates, the median and average numbers of ARGs per isolate were 7 and 7.3, respectively. In total, 42 resistance-conferring SNPs were detected in a total of 31 genomes. Among the genomes in which these SNPs were detected, the maximum number of SNPs detected was five and the median was 1.
There was a total of 341 aminoglycoside, 140 tetracycline, 134 sulfonamide, 115 β-lactam, 50 phenicol, 10 macrolide-lincosamide-streptogramin B (MLS), five fosfomycin, and one fluoroquinolone resistance genes detected in all the MDR and R genomes (Table 1). Colistin, fusidic acid, glycopeptide, nitroimidazole, oxazolidinone, and rifampicin resistance genes were not detected in any of the genomes. In total, there were 109 isolates that encoded aminoglycoside ARGs, and 101 of these encoded more than one aminoglycoside ARG. There were only 32, 27, and 18 isolates that encoded more than one sulfonamide, β-lactam, or tetracycline ARG, respectively. The ten most frequently detected ARGs, in order of decreasing frequency, were aph(6)-Id (94 isolates), aph(3″)-Ib (93 isolates), sul2 (90 isolates), tetB (66 isolates), blaCMY-2 (65 isolates), aph(3′)-Ia (61 isolates), tetA (58 isolates), sul1 (40 isolates), floR (39 isolates), blaTEM-1B (34), and aadA1 (22 isolates). Multiple transferrable ARGs conferring resistance or reduced susceptibility to antibiotics critical to human health were identified among the MDR isolates. These include the ESBLs blaCMY-2, blaCTX-M-1, blaCTX-M-14, blaCTX-M-15, blaTEM-214, macrolide resistance genes mphA, mphB, and the fluoroquinolone resistance gene aac(6′)-Ib-cr.
Point mutations in housekeeping genes that conferred resistance to antibiotics were also identified among the isolates (Table 1). Specifically, two mutation types were observed in gyrA (gyrA p.S83L and gyrA p.D87N), four in parC (parC p.A56T, parC p.S57T, parC p.S80I, parC p.E84K), one in parE (parE p.S458A), and two in the ampC promoter (ampC promoter n.-32T>A and n.-42C>T). Non-synonymous mutations in gyrA, parC, and parE are known to confer resistance to fluoroquinolones. Of these, the two most abundant were gyrA p.S83L and parC p.A56T, and they were identified in six isolates each. In total, 18 genomes encoded SNPs in the ampC promoter, and none of these encoded SNPs in gyrA, parC, or parE. Six isolates encoded the gyrA p.S83L mutation, and three of these encoded the gyrA p.D87N mutation. Four of the six isolates with a gyrA mutation also encoded mutations in parC, and one of these encoded mutations in parE. Eleven isolates encoded parC mutations, with six of them having parC p.A56T, four having parC p.S80I, three having parC p.S57T, and one having parC p.E84K. The latter isolate simultaneously encoded parC p.A56T and parC p.S80I. One isolate encoded parE p.S458A, and this isolate also encoded gyrA p.S83L, gyrA p.D87N, and parC p.S80I. Of the 31 isolates encoding these SNPs, 29 were the MDR genotype, one encoded one other ARG, and one encoded no other ARGs.

3.2. Biocide and Metal Resistance Genes

Transferrable biocide resistance genes (BRGs) and metal resistance genes (MRGs) were identified in many genomes; MDR genomes typically encoded more of these resistance genes than R or S genomes (Table 1). For each resistance category (MDR, R, and S), at least two genomes encoded copper resistance genes (pco), with five MDR genomes encoding this operon. Ten genomes encoded silver resistance genes (sil). The majority of the mercury resistance-encoding genomes were MDR (43 genomes) compared with R and S genomes (1 genome each). Similarly, the biocide resistance gene, qacEΔ, was found in 42 MDR genomes and 2 R genomes, but it was not found in any S genomes.

3.3. Co-Occurrence between ARGs, MRGs, and BRGs

In total, there were 222 positive co-occurrences between and among the identified ARGs, BRGs, and MRGs, and only three negative co-occurrences (Figure 1; Supplementary File S1). The most frequent co-occurrences between ARGs were aph(3″)-Ib-aph(6′)-Id, aph(3″)-Ib-sul2, and aph(6′)-Id-sul2. Azithromycin resistance gene, mphA, had positive co-occurrences with ARGs sul1, sul2, tetA, blaTEM-1B, and floR, as well as BRG qacE∆1 and MRG mer. blaCMY-2 had positive co-occurrences with 18 other ARGs, as well as BRGs qacE∆1, qacG, sugE, and MRGs mer and chr. The most frequent co-occurrences between BRGs were sugE-qacE∆1 and sugE-qacE∆1. Both qacE∆1 and sugE had twenty positive co-occurrences with ARGs. qacE∆1 had the most co-occurrences with sul1, and sugE had the most co-occurrences with blaCMY-2. The only co-occurrences between individual MRGs were mer-ter and mer-chr. Mercury resistance genes (mer) had 20 positive co-occurrences with ARGs as well as sugE and ter. Chromate resistance genes (chr) had positive co-occurrence with 10 ARGs, and tellurium resistance (ter) had positive co-occurrences with two ARGs, aadA2 and dfrA12. The only observed negative co-occurrences were between tetC and aph(3″)-Ib, aph(6′)-Id, and sul2.

3.4. Plasmid Replicon Diversity

There were 708 total plasmid replicons comprising 42 different replicon types identified among the isolates (Table 2). The most frequently detected replicon was IncFIB(AP001918), which was identified in 170 isolates, followed by ColRNAI, IncFIA, IncI1_Alpha, IncFIC(FII), and IncA/C2, which were detected in 92, 87, 47, 37, and 32 genomes, respectively. For all resistance groups (MDR, R, and S), the IncFIB(AP001918) plasmid was the most frequently detected. In terms of the percentage of replicon presence, the greatest difference between MDR and S genomes was in IncFIB(AP001918), which was carried by 65% of S genomes and 40% of MDR genomes. Similarly, appreciable differences were identified in the carriage rates of IncFIC(FII), IncA/C2, and IncFIA between MDR and S genomes (19.1%, 15.8%, and 11.9% difference between MDR and S genomes).

3.5. Genomic Diversity

In total, 142 STs were identified among the isolates, with ST10, ST58, ST88, and ST56 being the most frequently detected, which were identified 20, 18, 10, and 7 times, respectively (Table 1). Among the MDR isolates, ST10 was the most frequently detected ST (13 isolates). Among the susceptible isolates, ST58 was the most frequently detected ST (10 isolates). Among the isolates that were resistant, except for MDR, ST95 was the most frequently detected, followed by ST10 (three and two isolates, respectively). Within the MDR isolates, ST10 was the most frequently detected ST from pre- and post-weaned calves (ST56 was detected as many times as ST10 in post-weaned calves). ST88 was the most frequently detected ST among MDR isolates from lactating cows (five isolates). ST58 was the most frequently detected ST among MDR isolates from dry cows. Within the susceptible isolates, ST58 was the most frequently detected among lactating cow isolates, while ST164 was the most frequently detected among dry cow isolates; ST32 was the most frequently detected among pre-weaned calf isolates, and ST329 and ST2521 were the most frequently detected among post-weaned calf isolates.
Based on a phylogenetic comparison of the genomes with Escherichia genomes downloaded from NCBI, the isolates were classified into phylogroups A (53 isolates), B1 (139 isolates), B2 (4 isolates), C (16 isolates), D (26 isolates), E (13 isolates), F (4 isolates), and G (9 isolates) (Figure 2 and Figure 3; Table 1). Among the MDR group, isolates were classified as phylogroups B1, A, C, D, G, F, and E and were detected 44, 31, 13, 10, 5, 3, and 2 times, respectively. Among the resistant isolates, B1, A, D, E, B2, C, F, and G were detected 16, 6, 5, 3, 3, 1, 1, and 1 times, respectively. Among the susceptible isolates, B1, A, D, E, G, C, and B2 were detected 79, 16, 11, 8, 3, 2, and 1 times, respectively. MDR genomes were more likely to be phylogenetic groups A and C (residuals = 2.0 and 2.5, respectively), and S genomes were more likely to be phylogenetic group B1 (residual = 1.99; Chi-square test, χ2 = 46.629, p < 0.001).

3.6. Virulence and Fitness Factors

Genomes were interrogated for a broad suite of virulence and fitness factors (VFFs) that have both major and minor roles in pathogenesis, intra-host survival, and between-host transmission. In total, 49,407 VFFs were identified among the isolates, with multiple VFFs identified in all genomes (Supplementary File S2). The mean and median number of VFFs per isolate were 187 and 186, respectively. The highest number of VFFs identified in any isolate was 279, and the lowest was 114.
Multiple isolates with VFFs known to play significant roles in the pathogenesis of the major pathovars were detected (Figure 4). The sequences of nine strains (3.4% of the total) significantly aligned with the Shiga toxin genes of Shiga toxigenic E. coli (STEC). Six of these nine genomes encoded stx1A and stx1B, one encoded stx2A, three encoded stx2B, two encoded stx2d, and a single genome encoded stx1A, stx1B, stx2A, and stx2B. Among the STEC genomes, four encoded the intestinal adherence factor, intimin (eae), which is integral in STEC pathogenesis, indicating that these isolates were potential enterohemorrhagic E. coli (EHEC). Two of these, O103:H2 and O45:H2, are considered adulterants by the USDA Food Safety and Inspection Service [33]. Based on the presence of eae in their genomes, 16 isolates were determined to be enteropathogenic E. coli (EPEC). Of these, two were genotypically resistant, five were MDR, and nine were susceptible. Two MDR genomes and two susceptible genomes encoded the heat-stable enterotoxin estIa gene (STa) of enterotoxigenic E. coli (ETEC), but these did not encode the LT heat-labile toxin. Four isolates were characterized as uropathogenic E. coli (UPEC) based on the presence of chuA (heme-binding protein), fyuA (yersiniabactin receptor), and vat (autotransporter serine protease toxin). Two of these were MDR ST117, and two were resistant ST95 [34]. In total, 41 isolates (15% of the total) were identified as extraintestinal pathogenic E. coli (ExPEC) based on the presence of at least two of the following: VFs pap (P fimbriae), sfa/foc (S and F1C fimbriae), afa/draBC (Dr binding adhesins), kpsM (group 2 capsule), and iutA (aerobactin receptor) in their genomes. Thirty-four of these isolates were MDR; three were resistant, and four were susceptible. Among these ExPEC isolates, 16 different STs were identified, with ST10, ST88, and ST973 being the most frequently detected. Multiple other ExPEC genes were detected, such as iroN (salmochelin siderophore receptor), ibeABC (invasin of brain endothelial cells), sitABC (iron transport protein), cnf (cytotoxic necrotizing factor), cdt (cytolethal distending toxin), and pic (serine protease autotransporter) (Figure 4, Supplementary File S2). In total, 60 isolates (22%) were members of STs that are among the most common causes of ExPEC infections, including ST10, ST23, ST38, ST58, ST69, ST88, ST95, ST117, and ST167.

3.7. Accessory Genes Associated with the MDR and Susceptible Genotypes

The total gene content of the MDR and S genomes were compared to identify differences in accessory genes between these two groups of isolates. A non-metric multidimensional scaling (NMDS) analysis and an analysis of similarities (anosim) test demonstrated that the gene content of MDR genomes was different than that of S genomes (Figure 5). When all ARGs were removed from this analysis, this relationship remained statistically significant (anosim R = 0.16, p < 0.001), indicating that MDR genomes and susceptible genomes were slightly, yet significantly, different from each other, and these differences were not due to the presence of ARGs (Figure 5). There was no difference in the gene content of MDR E. coli isolated from calves than those isolated from adult cows (anosim p = 0.972), indicating that the gene contents of MDR strains shed by cows were not significantly different than those shed by calves (Figure 6).
There was a total of 766 accessory genes that were significantly enriched in either MDR strains or in susceptible strains (Fisher’s Exact Test, q < 0.05) (Figure 7; Supplementary File S3). Of these, 619 (80%) were enriched in MDR strains, and 147 were enriched in susceptible strains. Thirteen of the 619 accessory genes that were enriched in MDR strains were identified as ARGs. Signal proteins (markers of secreted proteins) were detected in 86 protein products of the enriched genes in MDR strains (Figure 7; Supplementary File S3). When the enriched genes in the susceptible strains were translated, 22 signal proteins were detected.
VFFs were also identified among the accessory genes enriched in either MDR or S genomes (Supplementary File S3). In the S genomes, these included cfaC (Mat/Ecp fimbriae outer membrane usher protein), cfaB (fimbrial protein), fimC (fimbrial chaperone protein), and fimI (long polar fimbria major subunit LpfA). In the MDR genomes, these included afa (adhesin), f17c-a (major type 1 subunit fimbrin), f17d-C (outer membrane usher protein), iuc-iutA (aerobactin synthesis and receptor), orgA (type III secretion apparatus protein OrgA/MxiK), pap (P-fimbriae), sit (iron and manganese transport), tia (Tia invasion determinant), and yjaa (YjaA family stress response protein).
Of the 619 genes enriched in MDR strains, 238 (38%) were annotated as known protein-coding genes. When assigned to KEGG functional categories, 26.8% were assigned to the signaling and cellular processes category of the protein families; 14.7% were assigned to the environmental information processing category; 13.4% were assigned to the unclassified genetic information processing category; 11.7% were assigned to the genetic information processing category of the protein families; 8.8% were assigned to the carbohydrate metabolism category, and 4.2% were assigned to the unclassified metabolism category.
Notable genes of interest known to confer significant phenotypes on cells that encode them that were enriched in the MDR genome include multiple iron acquisition systems, such as iucABCD-iutA (aerobactin synthesis and receptor), fecABCD (iron transport operon), sitACD (involved in iron and manganese transport), papABCD (P fimbriae), myo-inositol catabolism and transport genes iolABCDEG-iatA, and ascorbate metabolism genes ulaABC (Table 3). Multiple metal and biocide resistance genes were also enriched in MDR genomes. These include resistance to mercury (mer), copper (pco), silver (sil), and quaternary ammonia compounds (qacEΔ1) (Supplementary File S3).

4. Discussion

Results of this study demonstrate that genotypically antimicrobial-resistant and virulent E. coli are shed by dairy animals of all ages. Genes integral in the infection processes of all the major pathovars were detected among the strains. In previous studies, non-STEC strains isolated from bovine sources were frequently considered non-type-specific E. coli. However, a deeper genomic investigation of the strains in this study demonstrates that they often encode multiple VFFs as well as ARGs, demonstrating their human and animal health significance. Among these E. coli, STEC adulterant and ExPEC strains were repeatedly isolated. ExPEC strains are frequently MDR [35], and a high percentage of MDR strains in this study encoded ExPEC VFs, more so than the integral VFs of other pathovars.
Multiple ARGs conferring resistance to antimicrobials of human significance, particularly β-lactamases (blaCMY and blaCTX-M) and azithromycin (macrolide) resistance genes (mphA and mphB), along with point mutations conferring resistance to ciprofloxacin were identified in the genomes of E. coli isolated from the feces of dairy animals. β-lactams are among the most frequently used antibiotics in human clinical medicines, and resistance to these therapeutics has been increasing globally [36,37]. Fieldwork on these study farms demonstrated the presence of E. coli resistant to these antibiotics in the majority of farms, indicating that they are prevalent in dairy systems in the geographic study region [1]. Interestingly, blaCTX-M and, in particular, blaCMY were identified in more than half of MDR isolates, indicating that they were a significant component of MDR E. coli in these environments. This is further evidenced by the frequent co-occurrence of blaCMY with other ARGs in the E. coli genomes.
Based on an analysis of E. coli and the resistomes of calf feces, a higher ratio of resistant to susceptible bacteria is present in pre-weaned calf feces than in the feces of older animals [1,16]. Cao et al. [1] demonstrated this high level of resistance in pre- and post-weaned calves compared to dry or lactating cows, with pre-weaned calf feces harboring more resistant E. coli and more MDR E. coli than post-weaned calf feces. Previous studies have indicated that ARBs from teat surfaces can contaminate colostrum, which might seed the calf gut with ARBs, and that changes in diet may be, in part, responsible for the decrease in resistance abundance in these young animals. However, calves fed colostrum replacer and milk replacer similarly harbor high levels of resistance [38] that decrease over time, suggesting that there might be a selective pressure for ARBs in the calf gut that results in relatively high abundance of these organisms in young animals.
Previous work has shown that the presence of ARGs is associated with the presence of biocide and metal resistance genes (BRGs and MRGs) and that they are often collocated on the same plasmids or mobile elements [39,40]. It has been postulated that the presence of trace metals in feed selects ARBs that have MRGs encoded in their genomes [41,42]. Similar associations between ARGs, MRGs, and BRGs were identified in this study, most notably between the MDR genotype and the mercury resistance operon and the BRG, sugE1. However, the results of this study further demonstrate that E. coli with the MDR genotype is more likely to encode multiple suites of non-MRG/non-BRG genes encoding traits that may select for these organisms even in the absence of antimicrobial therapy or trace metal/biocide exposure and that these genes may point toward potential intervention strategies to reduce the carriage of ARBs in the herd or individual animal groups.
Our analyses indicated that the accessory gene contents of MDR isolates were somewhat different from those of the susceptible isolates, even when ARGs were removed from the analyses. Further, the gene content of MDR isolates from calves was not significantly different from that of adult cows, although the ratio of resistant to susceptible isolates is higher in calves than in cows [1]. Previous work has demonstrated that calves and adult cows can harbor the same MDR E. coli [43]. These data indicate that there are some genes that are more abundant in MDR strains than susceptible strains and that the gene contents of these MDR strains isolated from calves are approximately similar to those isolated from adult cows. Several of these genes compose operons that are involved in metabolic mechanisms that may be involved in this high MDR E. coli carriage in the calf gut. Of particular interest is the high number of genes enriched in the MDR isolates that are involved in iron acquisition. Iron is a limiting nutrient that is integral in many essential cellular processes. In human pathogenic E. coli, iron acquisition mechanisms are frequently found in ExPEC isolates, which are commensal in the gut but potentially pathogenic in the extraintestinal environment [44]. These systems are required for ExPEC colonization outside of the human gut, and studies have shown that they are upregulated in extraintestinal environments where available iron is limited [45,46,47]. However, the possible roles of iron acquisition mechanisms in the non-human mammalian gut have not been resolved. Iron scavenging via siderophores chelates iron, which transports these compounds back to the cell. Many taxa encode siderophores in the core chromosome, as well as accessory siderophores such as the sit system, aerobactin production, and salmochelin. The calf gut environment is relatively iron-depleted, and the main source of nutrition is usually colostrum for the first two days, followed by milk, both of which have a low iron content compared to that of the diets of older animals, which consume mostly forages and grains [48]. We hypothesize that the presence of siderophore systems (iucABCD-iutA and sitABCD), which are expressed in low-iron environments and are enriched in MDR strains in dairy animals, may allow for these strains to outcompete susceptible strains that typically lack these accessory iron scavenging systems. Siderophores are expressed in low-iron environments as a competitive mechanism to acquire this essential nutrient [49,50,51,52]. In E. coli, these genes (iucABCD-iutA and sitABCD) are typically encoded on incF plasmids, which also frequently encode ARGs, BRGs, and MRGs. We hypothesize that the collocation of plasmid-borne siderophores and ARGs selects for the latter in the low iron environment of the calf gut. Similar associations have been shown in E. coli collected from veal calves, which are typically fed an iron-limited diet [53].
The presence of other genes not involved in iron scavenging that are enriched in MDR strains suggests that the selection of ARGs within the calf gut may be multifactorial. These genes include myo-inositol transport and catabolism genes. Inositol is a carbocyclic sugar that has multiple structural and signaling roles in both eukaryotes and prokaryotes. It is found in both cow’s milk and feeds, such as cereal grains in its phosphorylated form, inositol hexakisphosphate (InsP6), or phytate, while forages have considerably lower InsP6 concentrations. Homologs of these ORFs have been identified in S. enterica, which can utilize inositol as a sole carbon source in vitro, indicating that it has an influence on the survival and, possibly, persistence of strains encoding these genes in environments with available inositol [54]. The introduction of forages and grains as a “calf starter” diet roughly coincides with a decrease in the carriage of MDR strains at around two weeks, which continues through the post-weaning period, suggesting that changes in diet may alter the abundance of resistance in the gut [2]. However, these genes are typically located on the E. coli chromosome, while most ARGs harbored by E. coli are plasmid-borne. It is not clear if there is a synergistic relationship between chromosomal-encoded genes and plasmid-borne ARGs; this association needs further evaluation.
Genes representing other, less defined mechanisms were also enriched in the MDR isolates; they may also confer a selective advantage for these bacteria in the calf gut and, hence, may also represent potential intervention targets for resistance in all animal groups. A significant number of genes were annotated as hypothetical proteins, indicating that their functions are not yet known. It may be that some of these are non-functional, but multiple hypothetical proteins were predicted to be translocated across the cell membrane, which suggests that they may be involved in interactions with the extracellular environment, which could include the bovine gastrointestinal tract. Further work identifying the functions of these genes in vitro and in vivo would need to be conducted to determine if they play any significant role in the survival of MDR strains in the animal gut.
MDR E. coli are frequently shed from calves and cows throughout the duration of their lives. The abundance of these resistant bacteria typically peaks at around two to three weeks of life, but it is still relatively high after weaning. The first two to three weeks after birth coincides with the time during which calves are primarily fed a milk diet, after which consumption of a calf starter, which has a higher concentration of iron than milk, occurs more frequently as the calf ages. These results demonstrate a need to further evaluate the role of iron availability within the calf gut as a potential driver of the high abundance of AMR in the feces of young calves, which may reveal a relatively simple approach to reducing the carriage of MDR E. coli in the dairy calf gut. Such an approach could have One Health implications by mitigating or disrupting the flow of multidrug-resistant E. coli between dairy farms, animals, and the environment.

Supplementary Materials

The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/antibiotics12101559/s1, Supplementary File S1: Co-occurrence results between antimicrobial-resistance genes (ARGs), biocide resistance genes (BRGs), and metal resistance genes (MRGs). Supplementary File S2: Full virulence matrix of all study strains is used in this analysis. Supplementary File S3: Genes enriched in MDR and susceptible genes along with their corresponding E. coli NCBI protein ID, BRG/MRG, annotation, SignalP identity, and KEGG orthology (KO). Supplementary File S4: NCBI accession numbers of E. coli genomes sequenced for this study.

Author Contributions

B.J.H. designed and coordinated the study, analyzed the data, and prepared the manuscript; S.S. analyzed data; S.W.K. carried out sequencing and analyzed data; E.H. collected samples; J.A.S.V.K. edited and critically revised the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This project was funded by internal USDA-ARS funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

All genome sequencing data generated in this study are publicly available at NCBI (Supplementary File S4).

Acknowledgments

We would like to thank Jakeitha Sonnier and Laura Del Collo for their assistance with laboratory work. Mention of trade names or commercial products in this article is solely for providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Co-occurrence among antimicrobial resistance genes (ARGs), metal resistance genes (MRGs), and biocide resistance genes (BRGs). Blue = statistically significant positive co-occurrence between genes. Yellow = statistically significant negative co-occurrence between genes. Grey = random co-occurrence.
Figure 1. Co-occurrence among antimicrobial resistance genes (ARGs), metal resistance genes (MRGs), and biocide resistance genes (BRGs). Blue = statistically significant positive co-occurrence between genes. Yellow = statistically significant negative co-occurrence between genes. Grey = random co-occurrence.
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Figure 2. Maximum likelihood core genome phylogeny of study genomes (n = 264) and reference genomes (n = 94) of the major phylogenetic groups. The tree is rooted in E. albertii. Red = multidrug-resistant genomes. Orange = antimicrobial-resistant genomes. Blue = antimicrobial-susceptible genomes. The maximum likelihood tree was inferred using RaxML with 1000 bootstrap replicates. Bar represents number of substitutions per site.
Figure 2. Maximum likelihood core genome phylogeny of study genomes (n = 264) and reference genomes (n = 94) of the major phylogenetic groups. The tree is rooted in E. albertii. Red = multidrug-resistant genomes. Orange = antimicrobial-resistant genomes. Blue = antimicrobial-susceptible genomes. The maximum likelihood tree was inferred using RaxML with 1000 bootstrap replicates. Bar represents number of substitutions per site.
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Figure 3. Proportions (%) of multidrug-resistant (MDR), antimicrobial-resistant (R), and antimicrobial-susceptible (S) isolates within each phylogenetic group.
Figure 3. Proportions (%) of multidrug-resistant (MDR), antimicrobial-resistant (R), and antimicrobial-susceptible (S) isolates within each phylogenetic group.
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Figure 4. Presence/absence heatmap of virulence and fitness factors (VFFs) of the major pathovars. Blue = present. Red = absent. MLST = Multi-Locus Sequence Type.
Figure 4. Presence/absence heatmap of virulence and fitness factors (VFFs) of the major pathovars. Blue = present. Red = absent. MLST = Multi-Locus Sequence Type.
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Figure 5. Non-metric multidimensional scaling (NMDS) analysis of the presence and absence of genes in the genomes of all MDR and susceptible isolates in this analysis (k = 3; stress = 0.17; ANOSIM R = 0.16; p < 0.01). The centroid of each group (MDR or Susc) is labeled. MDR genomes are shown in red. S genomes are shown in blue.
Figure 5. Non-metric multidimensional scaling (NMDS) analysis of the presence and absence of genes in the genomes of all MDR and susceptible isolates in this analysis (k = 3; stress = 0.17; ANOSIM R = 0.16; p < 0.01). The centroid of each group (MDR or Susc) is labeled. MDR genomes are shown in red. S genomes are shown in blue.
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Figure 6. Non-metric multidimensional scaling (NMDS) analysis of the presence and absence of genes in the genomes of all MDR isolates from calves and adult cows (k = 3; stress = 0.15; ANOSIM R = −0.08; p = 0.972). The centroid of each group (MDR calf or MDR cow) is labeled. MDR calf genomes are shown in red. MDR cow genomes are shown in blue.
Figure 6. Non-metric multidimensional scaling (NMDS) analysis of the presence and absence of genes in the genomes of all MDR isolates from calves and adult cows (k = 3; stress = 0.15; ANOSIM R = −0.08; p = 0.972). The centroid of each group (MDR calf or MDR cow) is labeled. MDR calf genomes are shown in red. MDR cow genomes are shown in blue.
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Figure 7. Results of the Fisher’s Exact Test analysis of gene enrichment in MDR and susceptible (S) genomes. Light-blue on far-left column = genes enriched in S genomes. Orange = genes enriched in MDR genomes. For columns from 2 to 4: green = the corresponding gene is an antimicrobial resistance gene (ARG), metal resistance gene/biocide resistance gene (MRG/BRG), or virulence and fitness factor (VFF). For the last column, prediction of signal peptides of secreted proteins: blue = SP(Sec/SPI), brown = LIPO(Sec/SPII), black = TAT(Tat/SPI).
Figure 7. Results of the Fisher’s Exact Test analysis of gene enrichment in MDR and susceptible (S) genomes. Light-blue on far-left column = genes enriched in S genomes. Orange = genes enriched in MDR genomes. For columns from 2 to 4: green = the corresponding gene is an antimicrobial resistance gene (ARG), metal resistance gene/biocide resistance gene (MRG/BRG), or virulence and fitness factor (VFF). For the last column, prediction of signal peptides of secreted proteins: blue = SP(Sec/SPI), brown = LIPO(Sec/SPII), black = TAT(Tat/SPI).
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Table 1. Isolation source, phylogenetic group, multi-locus sequence type (MLST), antimicrobial resistance genes (ARGs) separated by antimicrobial class, antimicrobial resistance-conferring point mutations, metal resistance genes (MRGs), and biocide resistance genes (BRGs) identified among the study isolates. Ami = aminoglycosides, β-Lac = β-Lactams, Flu = fluoroquinolones, Fos = Fosfomycin, MLS = macrolide-lincosamide-streptogramin B, Phe = phenicols, Sul = sulfonamide, Tet = tetracyclines, Tri = trimethoprim. As = arsenic, Cu = copper, Hg = mercury, Ag = silver, Te = Tellurium. BRGs = Biocide resistance genes. QAC = quaternary ammonium compounds.
Table 1. Isolation source, phylogenetic group, multi-locus sequence type (MLST), antimicrobial resistance genes (ARGs) separated by antimicrobial class, antimicrobial resistance-conferring point mutations, metal resistance genes (MRGs), and biocide resistance genes (BRGs) identified among the study isolates. Ami = aminoglycosides, β-Lac = β-Lactams, Flu = fluoroquinolones, Fos = Fosfomycin, MLS = macrolide-lincosamide-streptogramin B, Phe = phenicols, Sul = sulfonamide, Tet = tetracyclines, Tri = trimethoprim. As = arsenic, Cu = copper, Hg = mercury, Ag = silver, Te = Tellurium. BRGs = Biocide resistance genes. QAC = quaternary ammonium compounds.
Isolate IDSample SourcePhylogenetic GroupMLSTAntimicrobial Resistance Genes (ARGs)Resistance Conferring Point MutationsMetal Resistance Genes (MRGs)BRGs
Amiβ-LacFluFosMLSPheSulTetTrigyrAparCparEampCAsCuHgAgTeChromatesugE1QAC
ARS-CC11185Postweaned calvesG9192aadA1,
aph(3′)-Ia, aadA2,
aph(6)-Id, aph(3″)-Ib		blaCMY-2 floRsul1, sul2tetB, tetAdfrA1, dfra12 ampC promoter n.-42C>T merA, merT, merR, merP, merC, merD, merE chrAsugE1qacE∆1
ARS-CC11186Post-weaned calvesA1434aph(3′)-Ia, aadA5,
aph(6)-Id, aph(3″)-Ib		blaCMY-2, blaTEM-1B floRsul1, sul2tetAdfrA17 parC p.A56T pcoA, pcoB, pcoC, pcoD, pcoE, pcoR, pcoS silA, silB, silC, silP, silR chrAsugE1qacE∆1
ARS-CC11187Pre-weaned calvesA4085aadA1 sul1 ampC promoter n.-42C>T merA, merT, merR, merP, merC, merD, merE qacE∆1
ARS-CC11188post-weaned calvesA10aph(3′)-Ia, aph(6)-Id, aph(3″)-IbblaTEM-1B, blaCMY-2 sul2tetB sugE1
ARS-CC11189lactating cattleC88aph(6)-Id, aph(3′)-Ia, aph(3″)-Ib sul2tetB ampC promoter n.-42C>T
ARS-CC11190lactating cattleB1641aph(3′)-IablaCMY-2 tetA pcoA, pcoB, pcoC, pcoD, pcoE, pcoR, pcoS silA, silB, silC, silP, silR
ARS-CC11191lactating cattleC88 blaCMY-2 sugE1
ARS-CC11192pre-weaned calvesA10aph(3′)-Ia, aph(6)-Id, aph(3″)-IbblaCMY-2 sul2tetB pcoA, pcoB, pcoC, pcoD, pcoE, pcoR, pcoS silA, silC, silP, silR
ARS-CC11193dry cowsB158aph(3′)-Ia, aph(6)-Id, aadA24, aac(3)-Via, aph(3″)-IbblaCMY-2, blaTEM-1B floRsul1, sul2tetB, tetA merA, merT, merR, merP, merC, merD, merE sugE1qacE∆1
ARS-CC11194lactating cattleA10aph(3′)-Ia, aph(6)-Id, aph(3″)-IbblaCMY-2 mphAfloRsul2tetA merA, merT, merR, merP, merC, merD, merE chrAsugE1qacG
ARS-CC11195post-weaned calvesB19190aph(3″)-Ib, aph(6)-Id, aadA2blaCMY-2 floRsul1, sul2tetAdfrA12 merA, merT, merR, merP, merC, merD, merE chrAsugE1qacE∆1
ARS-CC11196dry cowsA10 blaCTX-M1
ARS-CC11197lactating cattleA9189aph(3″)-Ib, aph(6)-Id, aadA2blaCMY-2 floRsul1, sul2tetAdfrA12 parC p.A56T merA, merT, merR, merP, merC, merD, merE chrAsugE1qacE∆1
ARS-CC11198pre-weaned calvesB158aph(6)-Id aph(3″)-IbblaCMY-2, blaTEM-1B sul2 dfrA5 merA, merT, merR, merP, merC, merD, merE sugE1
ARS-CC11199lactating cattleC88aac(3)-Via, aadA24, aph(6)-Id, aph(3″)-IbblaCMY-2, blaTEM-1B floRsul2tetA merA, merT, merR, merP, merC, merD, merE sugE1
ARS-CC11200post-weaned calvesB156aph(3″)-Ib, aph(3′)-Ia, aph(6)-Id, aadA2blaCMY-2 mphAfloRsul1, sul2tetA, tetB, tetMdfrA12 merA, merT, merR, merP, merC, merD, merE chrAsugE1qacE∆1, qacG
ARS-CC11201dry cowsD69 blaCMY-2 arsA, arsB, arsC, arsD sugE1
ARS-CC11202lactating cattleB19194 blaCMY-2 arsA, arsB, arsC, arsD sugE1
ARS-CC11203pre-weaned calvesB11049 blaCTX-M1 sul2tetA
ARS-CC11204post-weaned calvesG657 blaCMY-2 sugE1
ARS-CC11205dry cowsB14086aph(6)-Id, aph(3″)-IbblaCMY-2 floRsul2tetA merA, merT, merR, merP, merC, merD, merE sugE1
ARS-CC11206lactating cattleB19203aph(3″)-Ib, aph(6)-Id, aadA1, aac(3)-Via, aadA5 floRsul1, sul2tetAdfrA17 chrA qacE∆1
ARS-CC11207post-weaned calvesD2485 blaCMY-2 tetA sugE1
ARS-CC11208post-weaned calvesA10aac(3)-Via, aph(3″)-Ib, aph(6)-IdblaCMY-2 floRsul2tetA merT sugE1
ARS-CC11209pre-weaned calvesA2325aph(6)-Id, aadA1, aph(3′)-Ia, aph(3″)-IbblaCMY-2, blaTEM-1B sul1tetB merA, merT, merR, merP, merC, merD sugE1qacE∆1
ARS-CC11211dry cowsB1937aph(6)-Id, aph(3″)-Ib sul2tetB
ARS-CC11212post-weaned calvesB11123
ARS-CC11214pre-weaned calvesB175 fosA7.5
ARS-CC11215post-weaned calvesB1201aph(3′)-Ia
ARS-CC11216dry cowsB11125
ARS-CC11217post-weaned calvesB156aph(6)-Id, aph(3″)-IbblaTEM-1B sul2tetB
ARS-CC11218pre-weaned calvesD2946
ARS-CC11219pre-weaned calvesC88aph(3′)-Ia, aph(6)-Id, aph(3″)-Ib sul2tetB ampC promoter n.-42C>T
ARS-CC11220post-weaned calvesC9172aph(3″)-Ib, aph(6)-Id, aph(3′)-Ia floRsul2tetB ampC promoter n.-32T>A
ARS-CC11221dry cowsB16189
ARS-CC11222pre-weaned calvesB156aadA2, aph(3′)-Ia, aph(3″)-Ib, aph(6)-IdblaTEM-1B sul1, sul2tetAdfrA12 merA, merT, merR, merP, merC, merD, merE terY2, terY1, terW, terZ, terA, terB, terC, terD, terE, terF qacE∆1
ARS-CC11223post-weaned calvesA329
ARS-CC11224dry cowsB11049
ARS-CC11225dry cowsB12521
ARS-CC11226pre-weaned calvesC23aadA1, aph(3′)-Iia, aph(6)-Ic, aph(6)-Id, aph(3″)-Ib sul2tetBdfrA1 ampC promoter n.-42C>T terW, terZ, terA, terB, terC, terD, terE, terF
ARS-CC11227post-weaned calvesB11172
ARS-CC11228lactating cattleB1101aph(6)-Id, aph(3″)-Ib sul2tetB
ARS-CC11229pre-weaned calvesB24260
ARS-CC11230dry cowsA8935
ARS-CC11231lactating cattleA1101aph(6)-Id, aph(3″)-Ib sul2tetB
ARS-CC11232lactating cattleB156aph(6)-Id, aph(3″)-Ib sul2tetB
ARS-CC11233pre-weaned calvesB158aac(3)-Iid, aadA5blaTEM-1B sul1, sul2tetBdfrA17 chrA qacE∆1
ARS-CC11234post-weaned calvesE1140aph(6)-Id, aph(3″)-IbblaCMY-2 floRsul2tetA merA, merT, merR, merP, merC, merD, merE sugE1
ARS-CC11235dry cowsB295 tetC
ARS-CC11236lactating cattleB1937aph(6)-Id, aph(3″)-Ib sul2tetB
ARS-CC11237pre-weaned calvesD973aadA7, aph(3′)-Ia, aph(6)-Id, aph(3″)-IbblaCMY-2 sul1, sul2 merA, merT, merR, merP, merC, merD, merE sugE1qacE∆1
ARS-CC11238lactating cattleB1442aph(3″)-Ib,aph(6)-Id floRsul2tetA
ARS-CC11239post-weaned calvesA329aph(3′)-Ia, aph(3″)-Ib, aph(6)-Id sul2tetB terW, terZ, terA, terB, terC, terD, terE, terF
ARS-CC11240post-weaned calvesB1101aph(3′)-Ia, aph(6)-Id, aph(3″)-Ib sul2tetB
ARS-CC11241pre-weaned calvesA10aph(3′)-Ia, aph(6)-Id, aph(3″)-IbblaCMY-2 sul2tetB sugE1
ARS-CC11242post-weaned calvesB12522aph(6)-Id, aph(3″)-Ib sul2tetB
ARS-CC11243pre-weaned calvesE57aph(3′)-Ia, aadA5, aph(6)-Id, aac(3)-Iia, aadA1, rmtE, aph(3″)-IbblaCMY-2 mphBcatA1sul2,
sul1		tetM, tetAdfrA1, dfrA17gyrA p.S83L merA, merT, merR, merP, merC, merD, merE chrAsugE1qacE∆1
ARS-CC11244post-weaned calvesB1446aph(3′)-Ia, aadA2, aph(6)-Id, aph(3″)-IbblaTEM-1A sul1tetA merA, merC, merD, merE qacE∆1
ARS-CC11245dry cowsB156aph(6)-Id, aph(3″)-Ib sul2tetB
ARS-CC11246post-weaned calvesB11844
ARS-CC11247post-weaned calvesB1278aph(3″)-Ib, aph(6)-Id floRsul2tetA
ARS-CC11248lactating cattleB158aph(3′)-Ia, aph(6)-Id, aph(3″)-Ib sul2tetB
ARS-CC11249pre-weaned calvesA10aph(3′)-Ia, aph(6)-Id, aph(3″)-IbblaCMY-2, blaTEM-1B sul2tetB sugE1
ARS-CC11250pre-weaned calvesA9191aph(3′)-Ia, aph(6)-Id, aph(3″)-IbblaCMY-2 tetB sugE1
ARS-CC11251pre-weaned calvesA93aph(3″)-Ib, aph(6)-Id, aadA1 sul1,sul2tetBdfrA1gyrA p.S83L merA, merT, merR, merP, merC, merD, merE qacE∆1
ARS-CC11252post-weaned calvesA744aph(6)-Id, aph(3″)-IbblaTEM-1B mphAcatA1sul2tetBdfrA17gyrA p.S83L, gyrA p.D87NparC p.A56T, parC p.S80I, parC p.E84K merA, merT, merR, merP, merC, merD, merE
ARS-CC11253pre-weaned calvesC23aph(3″)-Ib, aph(6)-Id, aph(3′)-Ia, aadA1 sul2tetBdfrA1 ampC promoter n.-42C>T terW, terZ, terA, terB, terC, terD, terE, terF
ARS-CC11254post-weaned calvesB158aph(6)-Id, aph(3″)-Ib sul2tetB
ARS-CC11255post-weaned calvesA206aph(3′)-Ia, aph(3″)-Ib, aph(6)-Id, aadA2blaTEM-1B catA1, floRsul1, sul2tetAdfrA12 parC p.A56T merA, merT, merR, merP, merC, merD, merE terY2, terY1, terW, terZ, terA, terB, terC, terD, terE, terF qacE∆1
ARS-CC11256post-weaned calvesB1155aac(3)-Via, aadA24 floRsul1tetA qacE∆1
ARS-CC11257pre-weaned calvesG657
ARS-CC11258lactating cattleB1164aph(6)-Id, aph(3″)-Ib sul2tetB
ARS-CC11260post-weaned calvesB1155
ARS-CC11261dry cowsE4175
ARS-CC11262dry cowsB12163
ARS-CC11263dry cowsB1278aph(6)-Id, aph(3″)-IbblaTEM-1A floRsul2tetA
ARS-CC11264pre-weaned calvesB18185
ARS-CC11265dry cowsB113
ARS-CC11266dry cowsB14481
ARS-CC11267pre-weaned calvesB121aac(3)-Via, aph(3″)-Ib, aph(6)-IdblaCMY-2 floRsul2tetA merA, merT, merR, merP, merC, merD, merE terW, terZ, terA, terB, terC, terD, terE, terF sugE1
ARS-CC11268post-weaned calvesA6927aadA24, aac(3)-Via, aph(3″)-Ib, aph(6)-IdblaCMY-2 sul1, sul2tetA merA, merT, merR, merP, merC, merE sugE1qacE∆1
ARS-CC11269post-weaned calvesB295 tetC
ARS-CC11270dry cowsB156
ARS-CC11271pre-weaned calvesB16559
ARS-CC11272dry cowsG9192aph(6)-Id, aph(3′)-Ia, aph(3″)-Ib, aadA1 sul2tetBdfrA1 ampC promoter n.-42C>T
ARS-CC11273lactating cattleG9192aph(6)-Id, aph(3′)-Ia, aph(3″)-Ib, aadA1 sul2tetBdfrA1 ampC promoter n.-42C>T
ARS-CC11274lactating cattleB1316aph(6)-Id, aph(3″)-Ib sul2tetB
ARS-CC7050lactating cattleA617aadA5, aac(6′)-Ib-crblaCTX-M-15aac(6′)-Ib-cr mphAcatB3sul1, sul2tetAdfrA17gyrA p.S83L, gyrA p.D87NparC p.S80IparE p.S458A chrA qacE∆1
ARS-CC9092pre-weaned calvesA10aadA1, aph(3′)-Iia, aph(6)-Ic, aph(6)-Id, aph(3″)-IbblaTEM-1B, blaCMY-2 tetB pcoA, pcoB, pcoC, pcoD, pcoE, pcoR, pcoS silA, silB, silC, silP, silR sugE1
ARS-CC9095pre-weaned calvesC88aph(6)-Id, aph(3′)-Ia, aph(3″)-Ib sul2tetB ampC promoter n.-42C>T
ARS-CC9098post-weaned calvesC88aph(3′)-Ia, aph(3″)-Ib, aph(6)-Id sul2tetB ampC promoter n.-42C>T
ARS-CC9100post-weaned calvesB1641aac(3)-Via, aadA24, aph(3″)-Ib, aph(3′)-Ia, aph(6)-Id, aadA5blaTEM-1B, blaCMY-2 floRsul1, sul2tetM, tetAdfrA17 sugE1qacE∆1
ARS-CC9105dry cowsA48aadA5, aac(3)-Via, aph(3′)-Ia, rmtE, aph(6)-Id, aadA24, aph(3″)-IbblaTEM-1B, blaCMY-2 floRsul1, sul2tetM, tetAdfrA17 sugE1qacE∆1, qacG
ARS-CC9108pre-weaned calvesB19190aph(3″)-Ib, aph(6)-Id, aadA2blaCMY-2 floRsul1, sul2tetAdfrA12 merA, merT, merR, merP, merC, merD, merE chrAsugE1qacE∆1
ARS-CC9117dry cowsB158aph(3″)-Ib, aph(6)-IdblaCMY-2 floRsul2tetA
ARS-CC9119pre-weaned calvesB12522aph(3″)-Ib, aac(6′)-Iia, aph(6)-IdblaCMY-2, blaTEM-1B floRsul1, sul2tetA, tetB merA, merT, merR, merP, merC, merD, merE chrAsugE1qacE∆1
ARS-CC9127post-weaned calvesF457aph(3″)-Ib, aph(6)-IdblaCMY-2 floRsul2tetA sugE1
ARS-CC9128post-weaned calvesB1297 blaCMY-2 sugE1
ARS-CC9129dry cowsB1297 blaCMY-2 sugE1
ARS-CC9131pre-weaned calvesD69aph(3′)-Ia, aph(6)-Id, aph(3″)-IbblaCMY-2 floRsul2tetB arsA, arsB, arsC, arsD
ARS-CC9545pre-weaned calvesA10 blaTEM-1D tetA pcoA, pcoB, pcoC, pcoD, pcoE, pcoR, pcoS silA, silB, silC, silP, silR
ARS-CC9546pre-weaned calvesB158aph(3′)-Ia, aph(6)-Id, aph(3″)-Ib tetB
ARS-CC9550pre-weaned calvesE9188
ARS-CC9554pre-weaned calvesB121aac(3)-Iid, aadA2, aph(6)-Id, aph(3″)-IbblaTEM-1B mphA sul1, sul2 dfrA12 ampC promoter n.-42C>T merA, merT, merR, merP, merC, merD, merE terW, terZ, terA, terB, terC, terD, terE, terFchrA qacE∆1
ARS-CC9555pre-weaned calvesB158 blaCMY-2 sugE1
ARS-CC9557pre-weaned calvesB186aac(3)-Via, aph(3′)-Ia, aph(3″)-Ib, aph(6)-IdblaCMY-2, blaTEM-1B floRsul1, sul2tetA, tetM gyrA p.S83LparC p.S80I merA, merT, merR, merP, merC, merD, merE sugE1qacE∆1, qacG
ARS-CC9561pre-weaned calvesB14086aph(3′)-Ia, aph(6)-Id, aph(3″)-Ib sul2tetB
ARS-CC9564pre-weaned calvesD106aadA7, aph(3′)-IablaTEM-1B sul1tetA parC p.S57T arsA, arsB, arsC, arsD merA, merT, merR, merP, merD, merE qacE∆1
ARS-CC9565pre-weaned calvesA10
ARS-CC9567pre-weaned calvesE9195 tetA
ARS-CC9568pre-weaned calvesE5597
ARS-CC9570pre-weaned calvesA10aph(3″)-Ib, aph(3′)-Ia, aph(6)-Id, aph(4)-Ia, aac(3)-IV, aadA1blaCMY-2 floRsul2tetB, tet31, tetAdfrA1 sugE1
ARS-CC9573pre-weaned calvesB117 blaCTX-M-14 terW, terZ, terA, terB, terC, terD, terE, terF
ARS-CC9575pre-weaned calvesA744aph(3′)-Ia, aph(3′)-Iia, aadA5, aph(6)-Id, aph(3″)-IbblaTEM-214 mphAfloR, catA1sul1, sul2tetB, tetAdfrA17gyrA p.S83L, gyrA p.D87NparC p.A56T, parC p.S80I merA, merT, merR, merP, merD, merE chrA qacE∆1
ARS-CC9705lactating cattleB158
ARS-CC9706post-weaned calvesA10aadA13 sul1tetB merA, merT, merR, merP, merC, merD, merE qacE∆1
ARS-CC9707dry cowsA10aadA13 sul1tetB merA, merT, merR, merP. merC, merD,merE qacE∆1
ARS-CC9708pre-weaned calvesE1131
ARS-CC9709lactating cattleB158
ARS-CC9710post-weaned calvesA540 pcoA, pcoB, pcoC, pcoD, pcoE, pcoR,pcoS silA, silB, silC, silP, silR
ARS-CC9711lactating cattleA548
ARS-CC9712dry cowsB12280
ARS-CC9713pre-weaned calvesB1765 terW, terZ, terA, terB, terC, terD, terE, terF
ARS-CC9714lactating cattleB18393
ARS-CC9715lactating cattleB14038
ARS-CC9716lactating cattleB1109aadA1 sul1 merA, merT, merR, merP, merC, merD, merE qacE∆1
ARS-CC9717pre-weaned calvesA4087
ARS-CC9718dry cowsE9198
ARS-CC9719dry cowsB1164
ARS-CC9720pre-weaned calvesD2485
ARS-CC9721lactating cattleB1603 terY1, terW, terZ, terA, terB, terC, terD, terE, terF
ARS-CC9722lactating cattleB11079
ARS-CC9723pre-weaned calvesA342 fosA7.5 terW, terZ, terA, terB, terC, terD, terE, terF
ARS-CC9724dry cowsB17289
ARS-CC9725post-weaned calvesB16189
ARS-CC9726lactating cattleB1164
ARS-CC9727post-weaned calvesB1162
ARS-CC9728dry cowsB15221 fosA7.5
ARS-CC9730dry cowsB1442
ARS-CC9731pre-weaned calvesF1280 tetB
ARS-CC9732lactating cattleB11727
ARS-CC9733post-weaned calvesA685
ARS-CC9734lactating cattleB158
ARS-CC9735post-weaned calvesB158
ARS-CC9737post-weaned calvesG657
ARS-CC9738lactating cattleB11123
ARS-CC9739lactating cattleG657
ARS-CC9741lactating cattleB1327
ARS-CC9742pre-weaned calvesB121
ARS-CC9743lactating cattleB1154
ARS-CC9744post-weaned calvesA329
ARS-CC9745lactating cattleB1847
ARS-CC9746pre-weaned calvesD137 terW, terZ, terA, terB, terC, terD, terE, terF
ARS-CC9747lactating cattleB11611 terW, terZ, terA, terB, terC, terD, terE, terF
ARS-CC9748post-weaned calvesB19193aph(3′)-Ia
ARS-CC9749dry cowsD6599
ARS-CC9750pre-weaned calvesB1711
ARS-CC9751dry cowsC423
ARS-CC9752post-weaned calvesB1154
ARS-CC9753lactating cattleB1155
ARS-CC9755post-weaned calvesB1336
ARS-CC9756lactating cattleB1278
ARS-CC9757pre-weaned calvesD32 terW, terZ, terA, terB, terC, terD, terE, terF
ARS-CC9758dry cowsB12602
ARS-CC9759post-weaned calvesA409 arsA, arsB, arsC, arsD, arsR
ARS-CC9760post-weaned calvesC23
ARS-CC9761lactating cattleB158
ARS-CC9762dry cowsB175 fosA7.5
ARS-CC9763dry cowsB1164
ARS-CC9764post-weaned calvesB11308
ARS-CC9765lactating cattleA10
ARS-CC9766lactating cattleB158
ARS-CC9767lactating cattleB295
ARS-CC9768pre-weaned calvesD32 terW, terZ, terA, terB, terC, terD, terE, terF
ARS-CC9769lactating cattleB1937
ARS-CC9770pre-weaned calvesB117 terW, terZ, terA, terB, terC, terD, terE, terF
ARS-CC9771dry cowsB11704
ARS-CC9772pre-weaned calvesE1087 tetC
ARS-CC9773lactating cattleD1204
ARS-CC9774post-weaned calvesB12521
ARS-CC9775dry cowsB1711
ARS-CC9776lactating cattleB1847
ARS-CC9777post-weaned calvesB12521
ARS-CC9778lactating cattleD1204 tetC
ARS-CC9779post-weaned calvesB1392
ARS-CC9780lactating cattleA10
ARS-CC9781pre-weaned calvesB158
ARS-CC9782lactating cattleB19197
ARS-CC9783post-weaned calvesB15730 tetA
ARS-CC9784dry cowsD4624
ARS-CC9785pre-weaned calvesA361
ARS-CC9786lactating cattleA10
ARS-CC9788post-weaned calvesB1711
ARS-CC9789dry cowsD38
ARS-CC9790pre-weaned calvesB129 terW, terZ, terA, terB, terC, terD, terE, terF
ARS-CC9791lactating cattleB11246
ARS-CC9792pre-weaned calvesB11308 tetC
ARS-CC9793dry cowsB1300 terW, terZ, terA, terB, terC, terD, terE, terF
ARS-CC9794post-weaned calvesB1392
ARS-CC9795lactating cattleB11246
ARS-CC9796lactating cattleB19196 fosA7.5 tetC
ARS-CC9798lactating cattleA398 tetC arsB, arsD, arsC, arsD, asrRpcoA, pcoB, pcoC, pcoD, pcoR, pcoS
ARS-CC9799post-weaned calvesD3509 terY2, tertY1, terW, terZ, terA, terB, terC, terD, terE, terF
ARS-CC9800dry cowsB1155
ARS-CC9801pre-weaned calvesB122
ARS-CC9802lactating cattleB1101
ARS-CC9803pre-weaned calvesE7244
ARS-CC9804post-weaned calvesE118
ARS-CC9805lactating cattleB15973
ARS-CC9806post-weaned calvesB12521
ARS-CC9807lactating cattleB1187
ARS-CC9808dry cowsA10 pcoA, pcoB, pcoC, pcoD, pcoE, pcoR, pcoS silA, silB, silC, silP, silR
ARS-CC9809dry cowsB158
ARS-CC9810post-weaned calvesA329
ARS-CC9811lactating cattleA206 parC p.A56T
ARS-CC9812post-weaned calvesB17812
ARS-CC9813dry cowsB18860
ARS-CC9830dry cowsE4151
ARS-CC9832lactating cattleB1603
ARS-CC9834lactating cattleB1297
ARS-CC9835lactating cattleB158
ARS-CC9837lactating cattleB158
ARS-CC9840lactating cattleB14481
ARS-CC9842dry cowsD8651
ARS-CC9843lactating cattleB1336
ARS-CC9861pre-weaned calvesB12539
ARS-CC9862pre-weaned calvesA216 arsA, arsB, arsC, arsD, arsRpcoA, pcoB, pcoC, pcoD, pcoE, pcoR, pcoSmerA, merT, merR, merP, merC, merD, merEsilA, silB, silC, silP, silR
ARS-CC9022pre-weaned calvesD362aac(3)-Via, aph(3″)-Ib, aph(3′)-Ia, aph(6)-IdblaCMY-2, blaTEM-1B floRsul1, sul2tetA, tetB merR, merP, merD, merE sugE1qacE∆1, qacG
ARS-CC9023pre-weaned calvesA10aph(6)-Id, aadA1, aph(3′)-Ia, aph(3″)-IbblaCMY-2, blaTEM-1B tetB sugE1
ARS-CC9024pre-weaned calvesB1101aac(3)-Via, aph(3″)-Ib, aph(6)-IdblaCMY-2 floRsul2tetA, tetB sugE1
ARS-CC9025pre-weaned calvesC88aph(3′)-Ia, aph(6)-Id, aph(3″)-Ib sul2tetB ampC promoter n.-42C>T
ARS-CC9026pre-weaned calvesE219 blaCMY-2 tetA sugE1
ARS-CC9027pre-weaned calvesA1703 blaCMY-2 sugE1
ARS-CC9028lactating cattleB1515aph(6)-Id, aph(3′)-Ia, aph(3″)-IbblaTEM-1B, blaCMY-2 tetB arsA, arsB, arsC, arsD sugE1
ARS-CC9029pre-weaned calvesC1083aadA1, aph(3′)-IablaTEM-1A catA1sul1tetA merA, merT, merR, merC, merD, merE qacE∆1
ARS-CC9032pre-weaned calvesD973aadA7, aph(3′)-Ia, aph(6)-Id, aph(3″)-Ib, aadA1, aadA7blaCMY-2, blaTEM-1B catA1sul1, sul2tetBdfrA1 merA, merT, merR, merP, merC, merD, merE sugE1qacE∆1
ARS-CC9033lactating cattleC88aph(6)-Id, aph(3″)-IbblaCMY-2 sul2 dfrA8
ARS-CC9034lactating cattleB1101 blaTEM-1B tetA
ARS-CC9036post-weaned calvesD973aadA7, aadA7, aph(3′)-Ia, aph(6)-Id, aph(3″)-IbblaCMY-2 sul1, sul2tetB merA, merT, merR, merP, merC, merD, merE sugE1qacE∆1
ARS-CC9038post-weaned calvesB156aph(3′)-Ia, aadA2, aph(6)-Id, aph(3″)-IbblaTEM-1B sul1, sul2tetAdfrA12 merA, merT, merR, merP, merC, merD, merE terY2, terY1, terW, terZ, terA, terB, terC, terD, terE, terF qacE∆1
ARS-CC9039pre-weaned calvesA10aadA2, aph(3′)-Ia, aph(3″)-Ib, aph(6)-IdblaCMY-2, blaTEM-1B mphAfloRsul1, sul2tetA, tetB, tetMdfrA12 merT, merR, merP, merC, merD, merE chrAsugE1qcG2
ARS-CC9040post-weaned calvesB16345aadA2, aph(3′)-Ia, aph(6)-Id, aph(3″)-IbblaCMY-2 floRsul1, sul2tetA, tetBdfrA12 merA, merT, merR, merP, merC, merD, merE chrAsugE1qacE∆1
ARS-CC9041pre-weaned calvesD106aadA7, aph(3′)-IablaTEM-1B, blaCTX-M-1 mphA sul1tetA parC p.S57T arsA, arsB, arsC, arsD merA, merT, merR, merP, merC, merD, merE qacE∆1
ARS-CC9042lactating cattleB11252 blaCTX-M-1 sul2tetA
ARS-CC9043pre-weaned calvesB1602aph(3′)-Ia, aph(6)-Id, aph(3″)-IbblaTEM-1B tetB
ARS-CC9044post-weaned calvesG117aadA1, aadA5, aph(3′)-IablaCTX-M-14, blaTEM-1B mphAcatA1sul1, sul2,tetAdfrA17 merA, merT, merR, merP, merC, merD, merE chrA qacE∆1
ARS-CC9068pre-weaned calvesG117aph(3′)-Ia, aadA1, aadA2blaCMY-2, blaCTX-M-14 sul1, sul2tetAdfrA12 merA, merT, merR, merP, merC, merD, merE sugE1qacE∆1
ARS-CC9046pre-weaned calvesA10aac(3)-Via, aadA1, aph(6)-Id, aph(3″)-Ib, aph(3′)-Ia floRsul1, sul2tetB, tetA ampC promoter n.-42C>T qacE∆1
ARS-CC9049post-weaned calvesD714 blaCMY-2 sugE1
ARS-CC9050pre-weaned calvesF967aph(3′)-Ia, aph(6)-Id, aph(3″)-IbblaCMY-2, blaTEM-1B sul2tetB sugE1
ARS-CC9051dry cowsD106 blaCMY-2 parC p.S57T arsA, arsB, arsC, arsD sugE1
ARS-CC9052lactating cattleD973aph(3″)-Ib, aph(6)-Id, aadA1, aadA7blaCMY-2 catA1sul2, sul1tetBdfrA1 merA, merT, merR, merP, merC, merD, merE terY2, terY1, terW, terZ, terA, terB, terC, terD, terE, terF sugE1qacE∆1
ARS-CC9053lactating cattleC88aph(3′)-Ia, aph(6)-Id, aph(3″)-Ib sul2tetB ampC promoter n.-42C>T
ARS-CC9055post-weaned calvesA48aadA5, aph(3′)-Ia, aph(6)-Id, aph(3″)-IbblaCMY-2, blaTEM-1B sul2tetB, tetAdfrA17 sugE1
ARS-CC9056dry cowsA167aph(3′)-Ia, aph(6)-Id, aadA5, aph(3″)-IbblaCMY-2, blaTEM-1B floRsul2tetB, tetAdfrA17 ampC promoter n.-42C>T merA, merT, merR, merP, merC, merD, merE sugE1qacE∆1
ARS-CC9057post-weaned calvesA167aph(6)-Id, aadA5, aph(3′)-Ia, aph(3″)-IbblaCMY-2, blaTEM-1B floRsul2tetB, tetAdfrA17 ampC promoter n.-42C>T merA, merT, merR, merP, merC, merD, merE sugE1qacE∆1
ARS-CC9058lactating cattleD9199aph(6)-Id, aph(3″)-IbblaCMY-2 floRsul2tetA merA, merT, merR, merP, merC, merD, merE sugE1
ARS-CC9059post-weaned calvesB117aph(6)-Id, aph(3″)-IbblaCMY-2 floRsul2tetA merA, merT, merR, merP, merC, merD, merE terW, terZ, terA, terB, terC, terD, terE, terF sugE1
ARS-CC9060pre-weaned calvesD32aph(6)-Id, aph(3″)-IbblaCMY-2 sul2tetA merA, merT, merR, merP, merC, merD, merE terW, terZ, terA, terB, terC, terD, terE, terF sugE1
ARS-CC9061dry cowsF1280aph(3″)-Ib, aph(6)-IdblaCMY-2 floRsul2tetB, tetA merA, merT, merR, merP, merC, merD, merE sugE1
ARS-CC9062pre-weaned calvesA34aadA1, aph(3′)-Ia, aph(6)-Id, aph(3″)-IbblaCMY-2, blaTEM-1B sul2tetBdfrA1 sugE1
ARS-CC9063lactating cattleC88aph(3′)-Ia, aph(6)-Id, aph(3″)-Ib sul2tetB ampC promoter n.-42C>T
ARS-CC9064pre-weaned calvesB1940aadA24, aph(3″)-Ib, aph(6)-IdblaCTX-M-14, blaOXA-1 catA1sul2tetBdfrA1 pcoA, pcoB, pcoC, pcoD, pcoE, pcoR, pcoS silA, silB, silC, silP, silR
ARS-CC9065lactating cattleB1940aadA1, aph(3″)-Ib, aph(6)-IdblaCTX-M-14, blaOXA-1 catA1sul2tetBdfrA1 pcoA, pcoB, pcoC, pcoD, pcoE, pcoR, pcoS silA, silB, silC, silP, silR
Table 2. Isolation source, phylogenetic group, sequence type (MLST), resistance group (MDR = multidrug-resistant; R = antimicrobial-resistant; S = antimicrobial-susceptible), plasmid replicons identified in study genomes.
Table 2. Isolation source, phylogenetic group, sequence type (MLST), resistance group (MDR = multidrug-resistant; R = antimicrobial-resistant; S = antimicrobial-susceptible), plasmid replicons identified in study genomes.
Isolate IDSample SourcePhylogenetic GroupMLSTResistance GroupPlasmid Replicons
ARS-CC11185postweaned calvesG9192MDRColRNAI, IncA/C2, IncFIA, IncFIB(AP001918), IncI1_Alpha
ARS-CC11186postweaned calvesA1434MDRIncA/C2, IncX1
ARS-CC11187preweaned calvesA4085MDRColRNAI, IncB/O/K/Z, IncFIB(AP001918), IncQ1
ARS-CC11188postweaned calvesA10MDRIncFIA, IncFIB(AP001918), IncFII, IncI1_Alpha
ARS-CC11189lactating cattleC88MDRCol(MG828), IncFIA, IncFIB(AP001918)
ARS-CC11190lactating cattleB1641MDRCol(MG828), Col440I, ColRNAI, IncFIB(AP001918), IncFII(pRSB107)_pRSB107, IncI1_Alpha, IncX1
ARS-CC11191lactating cattleC88RCol156, IncI1_Alpha
ARS-CC11192preweaned calvesA10MDRCol(MG828), Col(MP18), Col156, Col440I, ColRNAI, IncFIA, IncFIB(AP001918)
ARS-CC11193dry cowsB158MDRIncA/C2, IncFIB(AP001918)
ARS-CC11194lactating cattleA10MDRIncA/C2
ARS-CC11195postweaned calvesB19190MDRCol440I, ColRNAI, IncA/C2, IncFIB(AP001918), IncI1_Alpha
ARS-CC11196dry cowsA10RIncI1_Alpha, IncN
ARS-CC11197lactating cattleA9189MDRIncA/C2
ARS-CC11198preweaned calvesB158MDRIncFIB(AP001918), IncFII
ARS-CC11199lactating cattleC88MDRCol(MG828), Col8282, ColRNAI, IncA/C2, IncFIB(AP001918), IncFII, IncI1_Alpha
ARS-CC11200postweaned calvesB156MDRIncA/C2
ARS-CC11201dry cowsD69RIncFII
ARS-CC11202lactating cattleB19194RIncFII
ARS-CC11203preweaned calvesB11049MDRIncFIB(AP001918), IncI1_Alpha
ARS-CC11204postweaned calvesG657RColRNAI, IncFIB(AP001918), IncI1_Alpha
ARS-CC11205dry cowsB14086MDRColRNAI, IncA/C2, IncFIA, IncFIB(AP001918)
ARS-CC11206lactating cattleB19203MDRColRNAI, IncFII, p0111
ARS-CC11207postweaned calvesD2485RIncFIA, IncFIB(AP001918), IncI1_Alpha
ARS-CC11208postweaned calvesA10MDRIncA/C2
ARS-CC11209preweaned calvesA2325MDRCol440II, ColRNAI, IncFIB(AP001918), IncI1_Alpha
ARS-CC11211dry cowsB1937MDRColRNAI, IncFIB(AP001918), IncFIC(FII)
ARS-CC11212postweaned calvesB11123SIncFIB(pB171)_pB171
ARS-CC11214preweaned calvesB175RColRNAI, IncFIA, IncFIB(AP001918), IncFIC(FII), p0111
ARS-CC11215postweaned calvesB1201RIncFIB(AP001918), IncI1_Alpha, IncX1
ARS-CC11216dry cowsB11125SIncFIB(AP001918), IncFIC(FII)
ARS-CC11217postweaned calvesB156MDRColRNAI, IncY
ARS-CC11218preweaned calvesD2946SCol440I, IncFIB(AP001918)
ARS-CC11219preweaned calvesC88MDRIncFIA, IncFIB(AP001918)
ARS-CC11220postweaned calvesC9172MDRIncFII(pCoo)_pCoo
ARS-CC11221dry cowsB16189SIncFIA, IncFIB(AP001918), IncFIC(FII), IncY
ARS-CC11222preweaned calvesB156MDRIncFIB(AP001918), IncHI2A, IncHI2, RepA_pKPC-CAV1321
ARS-CC11223postweaned calvesA329SColRNAI, IncFIB(AP001918), IncFIC(FII), IncX1, IncY
ARS-CC11224dry cowsB11049S
ARS-CC11225dry cowsB12521SIncFIB(AP001918), IncX1
ARS-CC11226preweaned calvesC23MDRColRNAI, IncFIB(AP001918)
ARS-CC11227postweaned calvesB11172SCol156, ColRNAI, IncFIB(AP001918), IncFIC(FII), IncX1, IncX3
ARS-CC11228lactating cattleB1101MDRIncFIA(HI1)_HI1, IncFIB(pB171)_pB171
ARS-CC11229preweaned calvesB24260SIncFIB(AP001918)
ARS-CC11230dry cowsA8935SColRNAI, IncFIC(FII), IncI1_Alpha
ARS-CC11231lactating cattleA1101MDRColRNAI, IncFIB(AP001918), IncFIC(FII), IncFII
ARS-CC11232lactating cattleB156MDR
ARS-CC11233preweaned calvesB158MDRColRNAI, IncI2_Delta
ARS-CC11234postweaned calvesE1140MDRColRNAI, IncA/C2
ARS-CC11235dry cowsB295RColRNAI, IncFIB(AP001918), IncX1
ARS-CC11236lactating cattleB1937MDRIncFIB(AP001918), IncFIC(FII), IncI1_Alpha
ARS-CC11237preweaned calvesD973MDRIncFIA, IncFIB(AP001918)
ARS-CC11238lactating cattleB1442MDRIncFIA, IncFIB(AP001918), IncX1
ARS-CC11239postweaned calvesA329MDRIncFIB(AP001918)
ARS-CC11240postweaned calvesB1101MDRCol440I, ColRNAI, IncFIB(AP001918), IncFII(pHN7A8)_pHN7A8
ARS-CC11241preweaned calvesA10MDRIncFIA, IncFIB(AP001918)
ARS-CC11242postweaned calvesB12522MDRCol156
ARS-CC11243preweaned calvesE57MDRIncA/C2
ARS-CC11244postweaned calvesB1446MDRCol440I, IncFIB(AP001918)
ARS-CC11245dry cowsB156MDR
ARS-CC11246postweaned calvesB11844S
ARS-CC11247post-weaned calvesB1278MDRCol440I, ColRNAI
ARS-CC11248lactating cattleB158MDRCol8282, ColRNAI, ColpVC
ARS-CC11249preweaned calvesA10MDRIncFIA, IncFIB(AP001918), IncFII, IncI1_Alpha
ARS-CC11250preweaned calvesA9191MDRCol440I, IncFIA, IncFIB(pB171)_pB171, IncI_Gamma, IncX1
ARS-CC11251preweaned calvesA93MDRCol156, ColRNAI, IncB/O/K/Z, IncFIA, IncFIB(AP001918)
ARS-CC11252postweaned calvesA744MDRIncFIA, IncFIB(AP001918), IncFII(pAMA1167-NDM-5)_pAMA1167-NDM-5
ARS-CC11253preweaned calvesC23MDRColRNAI, IncFIB(AP001918)
ARS-CC11254postweaned calvesB158MDRIncFIB(AP001918)
ARS-CC11255postweaned calvesA206MDRCol156, IncA/C2, IncFII(pSE11)_pSE11, IncHI2A, IncHI2, RepA_pKPC-CAV1321, p0111
ARS-CC11256postweaned calvesB1155MDRIncFIB(AP001918)
ARS-CC11257preweaned calvesG657SColRNAI, IncY
ARS-CC11258lactating cattleB1164MDRCol440I, ColRNAI, IncFIA, IncFIB(AP001918), IncI2_Delta
ARS-CC11260postweaned calvesB1155SIncFIB(AP001918), IncI1_Alpha
ARS-CC11261dry cowsE4175SColRNAI, IncFIA, IncFIB(AP001918)
ARS-CC11262dry cowsB12163S
ARS-CC11263dry cowsB1278MDRColRNAI, IncFIB(AP001918), IncFIC(FII)
ARS-CC11264preweaned calvesB18185SIncFIA, IncFIB(AP001918), IncX1
ARS-CC11265dry cowsB113SIncFIA, IncFIB(AP001918), IncFIC(FII)
ARS-CC11266dry cowsB14481SIncFIA, IncFIB(AP001918)
ARS-CC11267preweaned calvesB121MDRIncA/C2, IncB/O/K/Z, IncFIB(AP001918), IncY
ARS-CC11268postweaned calvesA6927MDRCol440I, IncA/C2, IncFIA, IncFIB(pB171)_pB171
ARS-CC11269postweaned calvesB295RIncFIB(AP001918), IncX1, IncY
ARS-CC11270dry cowsB156SCol(MG828), IncFIA, IncFIB(AP001918), IncFIC(FII), IncI1_Alpha
ARS-CC11271preweaned calvesB16559S
ARS-CC11272dry cowsG9192MDRColRNAI, IncFIA, IncFIB(AP001918), IncI1_Alpha
ARS-CC11273lactating cattleG9192MDRColRNAI, IncFIA, IncFIB(AP001918), IncI1_Alpha
ARS-CC11274lactating cattleB1316MDRColRNAI, IncFIB(AP001918)
ARS-CC7050lactating cattleA617MDRColRNAI, IncFIA, IncFIB(AP001918)
ARS-CC9092preweaned calvesA10MDRIncFII, IncR
ARS-CC9095preweaned calvesC88MDRIncFIA, IncFIB(AP001918)
ARS-CC9098postweaned calvesC88MDRIncFIA, IncFIB(AP001918)
ARS-CC9100postweaned calvesB1641MDRIncA/C2, IncX1, IncX3, IncX4, IncY
ARS-CC9105dry cowsA48MDRIncA/C2
ARS-CC9108preweaned calvesB19190MDRCol440I, ColRNAI, IncA/C2, IncFIB(AP001918)
ARS-CC9117dry cowsB158MDRIncFIB(AP001918), IncY
ARS-CC9119preweaned calvesB12522MDRIncA/C2
ARS-CC9127postweaned calvesF457MDRColRNAI, IncFII, IncI2_Delta
ARS-CC9128postweaned calvesB1297RColRNAI, IncA/C2, IncI1_Alpha
ARS-CC9129dry cowsB1297RColRNAI, IncI1_Alpha
ARS-CC9131preweaned calvesD69MDRColRNAI, IncFIA, IncFIB(AP001918), IncI1_Alpha
ARS-CC9545preweaned calvesA10RCol156, IncFIA, IncFIB(AP001918), IncI2_Delta, IncX3
ARS-CC9546preweaned calvesB158RIncFIA(HI1)_HI1, IncFIB(pB171)_pB171
ARS-CC9550preweaned calvesE9188SIncI1_Alpha
ARS-CC9554preweaned calvesB121MDRCol(MG828), ColRNAI, IncB/O/K/Z, IncFIB(AP001918), p0111
ARS-CC9555preweaned calvesB158RIncFIA(HI1)_HI1, IncFIB(pB171)_pB171, IncI1_Alpha
ARS-CC9557preweaned calvesB186MDRIncA/C2, IncY
ARS-CC9561preweaned calvesB14086MDRColRNAI, IncI2_Delta
ARS-CC9564preweaned calvesD106MDRIncFIA, IncFIB(AP001918)
ARS-CC9565preweaned calvesA10SColRNAI, IncFIB(pB171)_pB171
ARS-CC9567preweaned calvesE9195RIncFIB(AP001918)
ARS-CC9568preweaned calvesE5597SIncFIB(AP001918)
ARS-CC9570preweaned calvesA10MDRCol(MG828), Col440I, ColRNAI, IncA/C2, IncFIA, IncFIB(AP001918)
ARS-CC9573preweaned calvesB117RColRNAI, IncFIB(AP001918), IncFII
ARS-CC9575preweaned calvesA744MDRColRNAI, IncX1
ARS-CC9705lactating cattleB158SIncFIB(AP001918), IncFII(pHN7A8)_pHN7A8
ARS-CC9706postweaned calvesA10MDRColRNAI, IncFIA, IncFIB(AP001918), IncFII(pHN7A8)_pHN7A8, IncFII
ARS-CC9707dry cowsA10MDRColRNAI, IncFIA, IncFIB(AP001918), IncFII(pHN7A8)_pHN7A8, IncFII
ARS-CC9708preweaned calvesE1131SCol440I
ARS-CC9709lactating cattleB158SIncFIA, IncFIB(AP001918)
ARS-CC9710postweaned calvesA540S
ARS-CC9711lactating cattleA548SColRNAI, IncFIB(AP001918)
ARS-CC9712dry cowsB12280S
ARS-CC9713preweaned calvesB1765SIncFIC(FII)
ARS-CC9714lactating cattleB18393S
ARS-CC9715lactating cattleB14038SIncFIA, IncFIB(AP001918), IncFIC(FII)
ARS-CC9716lactating cattleB1109R
ARS-CC9717preweaned calvesA4087SIncFIA, IncFIB(AP001918)
ARS-CC9718dry cowsE9198SIncFIA, IncFIB(AP001918), IncFIC(FII)
ARS-CC9719dry cowsB1164SIncFIA, IncFIB(AP001918), IncFIC(FII)
ARS-CC9720preweaned calvesD2485SCol440I, ColRNAI, IncFIA, IncFIB(pB171)_pB171
ARS-CC9721lactating cattleB1603SColRNAI, IncFIA, IncFIB(AP001918)
ARS-CC9722lactating cattleB11079SColRNAI
ARS-CC9723preweaned calvesA342RCol(MG828), Col156, ColRNAI, IncFIB(AP001918)
ARS-CC9724dry cowsB17289SColRNAI, IncFIA, IncFIB(AP001918)
ARS-CC9725postweaned calvesB16189SIncFIA, IncFIB(AP001918), IncFIC(FII), IncY
ARS-CC9726lactating cattleB1164SIncFIA
ARS-CC9727postweaned calvesB1162SColRNAI, IncFIB(AP001918)
ARS-CC9728dry cowsB15221RIncFIA, IncFIB(AP001918), IncFIC(FII), IncY
ARS-CC9730dry cowsB1442SIncFIA, IncFIB(AP001918)
ARS-CC9731preweaned calvesF1280RColRNAI
ARS-CC9732lactating cattleB11727SIncFIB(AP001918)
ARS-CC9733postweaned calvesA685SIncI1_Alpha
ARS-CC9734lactating cattleB158SIncFIA, IncFIB(AP001918), IncFIC(FII)
ARS-CC9735postweaned calvesB158SIncFIB(AP001918)
ARS-CC9737postweaned calvesG657SIncFIB(AP001918)
ARS-CC9738lactating cattleB11123SIncFIA(HI1)_HI1, IncFIB(K)_Kpn3
ARS-CC9739lactating cattleG657SCol(MG828), IncB/O/K/Z, IncFIB(AP001918)
ARS-CC9741lactating cattleB1327SIncFIB(AP001918)
ARS-CC9742preweaned calvesB121SCol440I, IncB/O/K/Z, IncFIB(AP001918)
ARS-CC9743lactating cattleB1154SIncFIA, IncFIC(FII)
ARS-CC9744postweaned calvesA329SColRNAI, IncFIB(AP001918), IncX1, IncY
ARS-CC9745lactating cattleB1847SCol(MG828), ColRNAI, ColpVC, IncI1_Alpha
ARS-CC9746preweaned calvesD137SIncFIB(AP001918), IncY
ARS-CC9747lactating cattleB11611SIncFIB(AP001918), IncFII(pHN7A8)_pHN7A8
ARS-CC9748postweaned calvesB19193RColRNAI, IncFIB(AP001918)
ARS-CC9749dry cowsD6599SIncI1_Alpha
ARS-CC9750preweaned calvesB1711SIncFIB(AP001918)
ARS-CC9751dry cowsC423SColRNAI, IncFIA, IncFIB(AP001918)
ARS-CC9752postweaned calvesB1154SIncFIA, IncFIB(AP001918)
ARS-CC9753lactating cattleB1155SIncFIB(AP001918), IncI1_Alpha, IncX4
ARS-CC9755postweaned calvesB1336SIncFIB(AP001918), IncFIC(FII)
ARS-CC9756lactating cattleB1278SIncFIB(AP001918), IncFIC(FII), IncFII, IncI1_Alpha
ARS-CC9757preweaned calvesD32SIncFIB(AP001918)
ARS-CC9758dry cowsB12602SColRNAI, IncFIB(AP001918), IncI2_Delta, IncY
ARS-CC9759postweaned calvesA409SIncFIB(K)_Kpn3, IncY
ARS-CC9760postweaned calvesC23SCol440I, IncFIA, IncFIB(pB171)_pB171
ARS-CC9761lactating cattleB158SIncFIB(AP001918), IncFIC(FII), IncX1
ARS-CC9762dry cowsB175RColRNAI, IncFIA, IncFIB(AP001918), IncFIC(FII), IncFII(pCoo)_pCoo,
ARS-CC9763dry cowsB1164SIncFIA, IncFIB(AP001918)
ARS-CC9764postweaned calvesB11308SIncFIB(AP001918)
ARS-CC9765lactating cattleA10S
ARS-CC9766lactating cattleB158SCol440I, IncI1_Alpha, IncI2_Delta
ARS-CC9767lactating cattleB295RIncFIB(AP001918), IncX1
ARS-CC9768preweaned calvesD32SIncB/O/K/Z, IncFIB(AP001918)
ARS-CC9769lactating cattleB1937S
ARS-CC9770preweaned calvesB117SIncFIB(AP001918)
ARS-CC9771dry cowsB11704SColRNAI, IncFIB(AP001918), IncI1_Alpha
ARS-CC9772preweaned calvesE1087RIncFIB(AP001918), IncY
ARS-CC9773lactating cattleD1204SColRNAI, IncFIB(AP001918)
ARS-CC9774postweaned calvesB12521SCol440I, IncFIA, IncFIB(AP001918), IncX1, IncX4
ARS-CC9775dry cowsB1711SIncFIA, IncFIB(AP001918), IncFIC(FII)
ARS-CC9776lactating cattleB1847SCol440II, ColRNAI, ColpVC, IncI1_Alpha, p0111
ARS-CC9777postweaned calvesB12521SColRNAI, IncFIB(AP001918)
ARS-CC9778lactating cattleD1204RIncFIB(AP001918), IncI2_Delta, IncY
ARS-CC9779postweaned calvesB1392SIncFIA(HI1)_HI1, IncFIB(AP001918), IncFIC(FII)
ARS-CC9780lactating cattleA10SColRNAI, IncFIC(FII)
ARS-CC9781preweaned calvesB158SIncFIA(HI1)_HI1, IncFIB(pB171)_pB171, IncY
ARS-CC9782lactating cattleB19197SCol440I, ColRNAI, IncFIA, IncFIB(AP001918), IncFIC(FII), IncI2_Delta
ARS-CC9783postweaned calvesB15730RCol(MG828), Col440I, Col8282, ColRNAI, IncFII, IncN
ARS-CC9784dry cowsD4624SCol156, ColRNAI, IncFIA, IncFIB(AP001918), IncFIC(FII), IncI2_Delta
ARS-CC9785preweaned calvesA361S
ARS-CC9786lactating cattleA10SColRNAI, IncFIB(pB171)_pB171
ARS-CC9788postweaned calvesB1711SColRNAI, IncFIB(AP001918), IncI1_Alpha
ARS-CC9789dry cowsD38SIncFIA, IncFIB(AP001918), IncFIC(FII)
ARS-CC9790preweaned calvesB129SColRNAI, IncFIB(AP001918)
ARS-CC9791lactating cattleB11246SColRNAI, IncFIA, IncI1_Alpha
ARS-CC9792preweaned calvesB11308RIncFIB(pB171)_pB171
ARS-CC9793dry cowsB1300SCol156, IncFIB(AP001918)
ARS-CC9794postweaned calvesB1392SIncFIA(HI1)_HI1, IncFIB(AP001918), IncFIC(FII), IncI1_Alpha
ARS-CC9795lactating cattleB11246SColRNAI, IncFIA, IncI1_Alpha
ARS-CC9796lactating cattleB19196RIncFIB(AP001918), pENTAS02
ARS-CC9798lactating cattleA398RIncFIA, IncFII
ARS-CC9799postweaned calvesD3509SColpVC, IncA/C2, IncFII(pCoo)_pCoo, IncHI2A, IncHI2, RepA_pKPC-CAV1321
ARS-CC9800dry cowsB1155SColRNAI
ARS-CC9801preweaned calvesB122S
ARS-CC9802lactating cattleB1101SIncFIA, IncFIB(AP001918)
ARS-CC9803preweaned calvesE7244SIncFIB(AP001918)
ARS-CC9804postweaned calvesE118SColRNAI, IncFIB(AP001918)
ARS-CC9805lactating cattleB15973SColRNAI, IncFIA, IncFIB(AP001918)
ARS-CC9806postweaned calvesB12521SIncFIA(HI1)_HI1, IncFIB(pB171)_pB171
ARS-CC9807lactating cattleB1187SIncFIA, IncFIB(AP001918), IncY
ARS-CC9808dry cowsA10SCol440I
ARS-CC9809dry cowsB158SIncFIA, IncFIB(AP001918)
ARS-CC9810postweaned calvesA329SColRNAI, IncFIB(AP001918), IncI2_Delta
ARS-CC9811lactating cattleA206R
ARS-CC9812postweaned calvesB17812SColRNAI, IncFIB(AP001918), IncY
ARS-CC9813dry cowsB18860SIncFIA, IncFIB(AP001918), IncFIC(FII)
ARS-CC9830dry cowsE4151SIncFIA, IncFIB(AP001918)
ARS-CC9832lactating cattleB1603SCol156, Col440I, ColRNAI, IncFIB(AP001918), IncFIC(FII), IncI2_Delta
ARS-CC9834lactating cattleB1297SIncFIA, IncFIB(AP001918)
ARS-CC9835lactating cattleB158SColRNAI, IncFIA, IncFIB(AP001918), IncFIC(FII), IncI_Gamma
ARS-CC9837lactating cattleB158SCol440I, IncY
ARS-CC9840lactating cattleB14481SIncFIA, IncFIB(AP001918)
ARS-CC9842dry cowsD8651SIncY
ARS-CC9843lactating cattleB1336SIncFIA, IncFIB(AP001918)
ARS-CC9861preweaned calvesB12539SIncFIA, IncFIB(AP001918), IncI1_Alpha
ARS-CC9862preweaned calvesA216SCol440II, Col440I, IncFIA(HI1)_HI1, IncFIB(K)_Kpn3, IncHI1A, IncHI1B(R27)_R27
ARS-CC9022preweaned calvesD362MDRCol156, ColRNAI, IncA/C2, IncFIA, IncFIB(AP001918)
ARS-CC9023preweaned calvesA10MDRIncFIB(AP001918), IncI1_Alpha
ARS-CC9024preweaned calvesB1101MDRIncA/C2, IncFIA(HI1)_HI1, IncFIB(pB171)_pB171
ARS-CC9025preweaned calvesC88MDRColRNAI, IncFIA, IncFIB(AP001918)
ARS-CC9026preweaned calvesE219RIncY
ARS-CC9027preweaned calvesA1703RIncFII, IncQ1
ARS-CC9028lactating cattleB1515MDRIncFIB(AP001918), IncI1_Alpha
ARS-CC9029preweaned calvesC1083MDRIncFIB(AP001918), IncI2_Delta
ARS-CC9032preweaned calvesD973MDRIncB/O/K/Z, IncFIA, IncFIB(AP001918)
ARS-CC9033lactating cattleC88MDRColRNAI, IncFII, IncI1_Alpha
ARS-CC9034lactating cattleB1101RIncFIB(AP001918), IncFIC(FII), IncX1, IncX3
ARS-CC9036postweaned calvesD973MDRIncFIA, IncFIB(AP001918)
ARS-CC9038postweaned calvesB156MDRIncFIB(AP001918), IncHI2A, IncHI2, RepA_pKPC-CAV1321
ARS-CC9039preweaned calvesA10MDRIncA/C2, IncFIB(AP001918), IncI2_Delta, IncX1
ARS-CC9040postweaned calvesB16345MDRIncY
ARS-CC9041preweaned calvesD106MDRIncFIA, IncFIB(AP001918), IncI1_Alpha, IncN
ARS-CC9042lactating cattleB11252MDRIncFIB(AP001918), IncFIC(FII), IncI1_Alpha
ARS-CC9043preweaned calvesB1602MDRIncFIB(AP001918), IncY
ARS-CC9044postweaned calvesG117MDRCol(MG828), Col440I, ColRNAI, IncFIA, IncFIB(AP001918), IncFII
ARS-CC9068preweaned calvesG117MDRCol8282, ColRNAI, IncFIA, IncFIB(AP001918), IncFII
ARS-CC9046preweaned calvesA10MDRIncFIA, IncFIB(AP001918), IncI1_Alpha
ARS-CC9049postweaned calvesD714RIncFIB(AP001918), IncFII, IncI2_Delta
ARS-CC9050preweaned calvesF967MDRIncFIA, IncFIB(AP001918), IncI1_Alpha, IncI2_Delta
ARS-CC9051dry cowsD106RColRNAI, IncI1_Alpha
ARS-CC9052lactating cattleD973MDRIncFIA, IncFIB(AP001918), IncHI2A, IncHI2, IncI1_Alpha, RepA_pKPC-CAV1321
ARS-CC9053lactating cattleC88MDRIncFIA, IncFIB(AP001918)
ARS-CC9055postweaned calvesA48MDRIncFIB(AP001918), IncFIC(FII), IncI1_Alpha, IncR, IncY
ARS-CC9056dry cowsA167MDRCol(MG828), Col156, ColRNAI, IncA/C2, IncFIA, IncFIB(AP001918), IncY
ARS-CC9057postweaned calvesA167MDRCol(MG828), Col156, ColRNAI, IncA/C2, IncFIA, IncFIB(AP001918), IncY
ARS-CC9058lactating cattleD9199MDRIncA/C2
ARS-CC9059postweaned calvesB117MDRCol(MG828), IncA/C2, IncFIB(AP001918)
ARS-CC9060preweaned calvesD32MDRIncA/C2, IncB/O/K/Z, IncFIB(AP001918)
ARS-CC9061dry cowsF1280MDRColRNAI, IncA/C2
ARS-CC9062preweaned calvesA34MDRCol(MG828), IncFIA, IncFIB(AP001918)
ARS-CC9063lactating cattleC88MDRIncFIA, IncFIB(AP001918), IncX4
ARS-CC9064preweaned calvesB1940MDRColE10, ColRNAI, IncFII
ARS-CC9065lactating cattleB1940MDRColE10, ColRNAI, IncFII
Table 3. Operons of interest that were enriched in MDR genomes. Also listed are the functions of these operons, the ranges of percent presence in MDR strains (not all genes within an operon were detected), maximum percent presence in susceptible strains, and the q-values indicating the statistical significance of their enrichment in MDR genomes (Fisher’s Exact Test).
Table 3. Operons of interest that were enriched in MDR genomes. Also listed are the functions of these operons, the ranges of percent presence in MDR strains (not all genes within an operon were detected), maximum percent presence in susceptible strains, and the q-values indicating the statistical significance of their enrichment in MDR genomes (Fisher’s Exact Test).
OperonFunctionCarried by MDR Strains (%)Carried by Susceptible Strains (%)q-Values
iucABCD-iutAAerobactin synthesis/receptor48%6%1.61 × 10−9
sitACDIron ABC transporter 28 to 42%8%1.71 × 10−6
papABCDEGHIJKP fimbriae30% to 53%11%7.99 × 10−5
fecABCDEFerric citrate transport system60 to 62%24%0.00016
iolABCDEG-iatAmyo-inositol transport and utilization22%3%0.0023
alsABCD-allose transport system 49%21%0.0087
ulaABCAscorbate transport50 to 56%26%0.013
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Haley, B.J.; Kim, S.W.; Salaheen, S.; Hovingh, E.; Van Kessel, J.A.S. Genome-Wide Analysis of Escherichia coli Isolated from Dairy Animals Identifies Virulence Factors and Genes Enriched in Multidrug-Resistant Strains. Antibiotics 2023, 12, 1559. https://doi.org/10.3390/antibiotics12101559

AMA Style

Haley BJ, Kim SW, Salaheen S, Hovingh E, Van Kessel JAS. Genome-Wide Analysis of Escherichia coli Isolated from Dairy Animals Identifies Virulence Factors and Genes Enriched in Multidrug-Resistant Strains. Antibiotics. 2023; 12(10):1559. https://doi.org/10.3390/antibiotics12101559

Chicago/Turabian Style

Haley, Bradd J., Seon Woo Kim, Serajus Salaheen, Ernest Hovingh, and Jo Ann S. Van Kessel. 2023. "Genome-Wide Analysis of Escherichia coli Isolated from Dairy Animals Identifies Virulence Factors and Genes Enriched in Multidrug-Resistant Strains" Antibiotics 12, no. 10: 1559. https://doi.org/10.3390/antibiotics12101559

APA Style

Haley, B. J., Kim, S. W., Salaheen, S., Hovingh, E., & Van Kessel, J. A. S. (2023). Genome-Wide Analysis of Escherichia coli Isolated from Dairy Animals Identifies Virulence Factors and Genes Enriched in Multidrug-Resistant Strains. Antibiotics, 12(10), 1559. https://doi.org/10.3390/antibiotics12101559

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