Evidence for Horizontal Transmission and Recirculation of Shiga Toxin-Producing Escherichia coli in the Beef Production Chain in South Africa Using Whole Genome Sequencing
Abstract
:1. Introduction
2. Materials and Methods
2.1. Sources of Isolates
2.1.1. Cattle Feedlots
2.1.2. Abattoir and Retail Outlets
2.1.3. Isolation of STEC Strains
2.1.4. Multiplex PCR to Identify Virulence
2.1.5. Validation of mPCR
2.2. Whole Genome Sequencing and Analysis
2.3. Phylogenetic Analysis of STEC Isolates
3. Results
3.1. Isolates
3.2. Multilocus Sequence Typing
3.3. Virulence Genes
3.4. Antimicrobial Resistance Genes
3.5. Phylogenetic Analysis
4. Discussion
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Lab id | Sample Type * | Source | Season ** | Location | Serogenotype *** | STEC | Adherence | Haemolysin |
---|---|---|---|---|---|---|---|---|
GdH35(2) | Faeces | abattoir | W | Gauteng east | H29 | stx2a, stx2b | eaeH | hlyE |
PaJ36(b) | perineum HS | abattoir | W | Gauteng north | H8 | stx1a, stx1b, stx2a, stx2d1A | eaeH | hlyA, hlyB, hlyC, hlyD, hlyE |
PcJ28(a) | perineum HS | abattoir | W | Gauteng north | O8:H19 | stx1a, stx1b, stx2a, stx2b | eaeH, ehaA | hlyA, hlyB, hlyC, hlyD, hlyE |
RaM39(1) | post-evisc CS | abattoir | W | Gauteng west | H19 | stx2a, stx2b | eaeH | hlyA, hlyB, hlyC, hlyD, hlyE |
RcM39(a) | post-evisc CS | abattoir | W | Gauteng west | H7 | stx1a, stx1b, stx2a, | eaeH, ehaA | hlyA, hlyB, hlyD, hlyE |
RaM23(1) | post-evisc CS | abattoir | S | Gauteng west | H2 | stx1a, stx1b, stx2a, | ehaA- | hlyA, hlyC, hlyD, hlyE |
RaN16(1) | post-evisc CS | abattoir | S | Gauteng west | H25 | stx1a, stx1b | eae, eaeH, tir, nleBI, nleB2 | hlyA, hlyB, hlyD, hlyE |
PbK3(b) | pre-evisc CS | abattoir | S | Gauteng north | H19 | stx2a, stx2b | eaeH | hlyA, hlyB, hlyC, hlyD, hlyE |
LS 92a | faeces | farm | S | Gauteng north | H7 | stx2a, stx2dB | eaeH | hlyE |
CX 104(3) | faeces | farm | S | Gauteng north | H25 | stx2a, stx2dB | eae, eaeH, ehaA, tir, nleBI | hlyA, hlyB, hlyD, hlyE |
LS2 66(2) | faeces | farm | S | Gauteng north | H19 | stx2a | eaeH | hlyE |
CX 57(1) | faeces | farm | S | Gauteng north | H8 | stx1a, stx1b, stx2b, stx2d1A | eaeH, ehaA | hlyA, hlyB, hlyC, hlyD, hlyE |
LS2 102-3b | faeces | farm | S | Gauteng north | O9:H2/H9 | stx1a, stx1b | eae, tir, nleB2-2 | hlyD, hlyE |
LS2 93c | faeces | farm | S | Gauteng north | H2 | stx1a, stx1b | eae, eaeH, tir, nleB2-2 | hlyA, hlyB, hlyC, hlyD, hlyE |
CX 101(1) | faeces | farm | S | Gauteng north | H2 | stx1a, stx1b | eae, eaeH, tir | hlyA, hlyB, hlyD, hlyE |
CX 102(1) | faeces | farm | S | Gauteng north | H2 | stx1a, stx1b | eae, eaeH, tir, nleBI | hlyA, hlyD, hlyE |
CX 103(4) | faeces | farm | S | Gauteng north | H2 | stx1a, stx1b | eae, eaeH, tir | hlyB, hlyD, hlyE |
LS 102c | faeces | farm | S | Gauteng north | H2 | stx1a, stx1b | eae, eaeH, tir | hlyB, hlyD, hlyE |
CX 8(4) | faeces | farm | S | Gauteng north | 0 | stx1a | eaeH, eaeX | 0 |
FAF 33(1) | faeces | farm-abattoir | S | Gauteng north | H7 | stx2b | eae, eaeH, tir, nleB2 | hlyD, hlyE |
FAF 8(8) | faeces | farm-abattoir | S | Gauteng north | H25 | stx2a, stx2dB | eae, eaeH, ehaA, tir | 0 |
FAF 85(1) | faeces | farm-abattoir | S | Gauteng north | H8 | stx1a, stx1b, stx2b, stx2d1A | eaeH | hlyA, hlyB, hlyC, hlyD, hlyE |
FAF 68(1) | faeces | farm-abattoir | S | Gauteng north | H2 | stx1a, stx1b, stx2a, stx2dB | eaeH, saa | hlyA, hlyB, hlyC, hlyD, hlyE |
FAF 68(a) | faeces | farm-abattoir | S | Gauteng north | H2 | stx1a, stx1b, stx2a, | eaeH | hlyA, hlyB, hlyC, hlyD, hlyE |
FAF 51(1) | faeces | farm-abattoir | S | Gauteng north | H25 | stx1a, stx1b | eae, eaeH, tir, nleB2 | hlyA, hlyB, hlyD, hlyE |
FA3 9B(1) | faeces | farm-env | S | Gauteng north | H29 | stx2b, stx2dB | eaeH | hlyE |
FA3 9B(3) | faeces | farm-env | S | Gauteng north | H29 | stx2b, stx2d1A, stx2dB | eaeH | hlyE |
SSL5(1) | biltong | retail | S | Gauteng north | H29 | stx2d1 | eaeH | hlyE |
WWL2(2) | boerewors | retail | S | Gauteng north | O8:H19 | stx2a, stx2dB | eaeH | hlyA, hlyB, hlyC, hlyD, hlyE |
WWL2(3) | boerewors | retail | S | Gauteng north | O8:H19 | stx2a, stx2dB | eaeH, saa | hlyA, hlyC, hlyD, hlyE |
KEL2(3) | boerewors | retail | A | Gauteng north | H19 | stx2a | eaeH | hlyE |
PSL1(3) | brisket | retail | A | Gauteng north | H12 | stx2a, stx2dB | - | hlyE |
PSL1(4) | brisket | retail | A | Gauteng north | O8:H19 | stx1a, stx1b, stx2a, stx2dB | eaeH, saa | hlyA, hlyB, hlyC, hlyD, hlyE |
Clonal Complex | Sample | Source | Location * | ST † | Serogenotype | stx-Subtypes |
---|---|---|---|---|---|---|
5 matching loci | Post-evisceration-RbM15-4 | abattoir | GW | ST1049 | H10 | - |
Pre-evisceration-PdK13-2 | abattoir | GN | ST155 | H21 | - | |
Faeces-GdH35-1 | abattoir | GE | ST58 | O8:H30 | - | |
5 matching loci | Brisket-PSL1-4 | retail | GN | ST201 | O8:H19 | stx1a, stx1b, stx2a, stx2dB |
Chilled-PaQ7-1 | abattoir | GN | ST162 | O8:H19 | - | |
Perineal-PcJ28-a | abattoir | GN | ST469 | O8:H19 | stx1a, stx1b, stx2a, stx2b | |
6 matching loci | Post-evisceration-PdM31-1 | abattoir | GN | ST1145 | H16 | - |
Pre-evisceration-PdK21-1 | abattoir | GN | ST10 | O6:H12 | - | |
Mince-PWNL3-2 | retail | GN | ST1141 | H4 | - |
Antimicrobial Class | Resistance Genes | No. of Isolates Positive for AMR Genes | Antimicrobial Compounds |
---|---|---|---|
Aminoglycosides | aph (3″)-Ib | 8 | Aminoglycoside |
aph (6)-Id | 8 | Aminoglycoside | |
aadA | 4 | Aminoglycoside | |
aadA2 | 2 | Aminoglycoside | |
aadA3 | 3 | Aminoglycoside | |
aadA4 | 1 | Aminoglycoside | |
kdpE | 83 | Aminoglycoside | |
Amphenicols | cmlA6 | 1 | Amphenicols |
floR/chloramphenicol | 3 | Amphenicols | |
Beta-lactam/beta-lactamase-inhibitor | ampC | 83 | Cephalosporin, penam |
TEM-1 | 2 | Penam, monobactam, penem, cephalosporin | |
TEM-150 | 1 | Penam, monobactam, penem, cephalosporin | |
Fluoroquinolones | patA | 84 | Fluoroquinolone |
Glycopeptides | bacA | 84 | Peptide |
eptA/PmrC | 85 | Peptide | |
pmrF | 85 | Peptide | |
ugd/pmrE | 73 | Peptide | |
yojI | 84 | Peptide | |
Macrolide | mphB | 4 | Macrolide |
Multidrug (MDR) efflux pumps | CRP | 85 | Penam, macrolide, fluoroquinolone |
acrA | 85 | Tetracycline, glycylcycline, rifamycin, phenicol, penam, cephalosporin, fluoroquinolone, disinfecting agents and antiseptics | |
emrE | 63 | Macrolide | |
mdfA | 84 | Disinfecting agents and antiseptics, tetracycline | |
H-NS | 83 | Macrolide, tetracycline, penam, cephalosporin, fluoroquinolone, cephamycin | |
acrB | 82 | Tetracycline, glycylcycline, rifamycin, phenicol, penam, cephalosporin, fluoroquinolone, disinfecting agents and antiseptics | |
acrD | 82 | Aminoglycoside | |
acrE | 82 | Penam, cephamycin, fluoroquinolone, cephalosporin | |
acrF | 79 | Penam, cephamycin, fluoroquinolone, cephalosporin | |
acrS | 80 | Tetracycline, cephamycin, glycylcycline, rifamycin, phenicol, penam, cephalosporin, fluoroquinolone, disinfecting agents and antiseptics | |
baeR | 85 | Aminocoumarin, aminoglycoside | |
baeS | 85 | Aminocoumarin, aminoglycoside | |
cpxA | 84 | Aminocoumarin, aminoglycoside | |
emrA | 85 | Fluoroquinolone | |
Antimicrobial Class | Resistance Genes | Number of Resistant Isolates | Antimicrobial Compounds |
Multidrug (MDR) efflux pumps | emrB | 85 | Fluoroquinolone |
emrK | 83 | Tetracycline | |
emrR | 85 | Fluoroquinolone | |
emrY | 79 | Tetracycline | |
evgA | 84 | Penam, tetracycline, macrolide, fluoroquinolone | |
evgS | 78 | Penam, tetracycline, macrolide, fluoroquinolone | |
gadW | 83 | Penam, macrolide, fluoroquinolone | |
gadX | 81 | Penam, macrolide, fluoroquinolone | |
marA | 85 | Tetracycline, glycylcycline, rifamycin, phenicol, penam, cephalosporin, cephamycin, penem, monobactam, carbapem, fluoroquinolone, disinfecting agents and antiseptics | |
mdtA | 84 | Aminocoumarin | |
mdtB | 84 | Aminocoumarin | |
mdtC | 84 | Aminocoumarin | |
mdtE | 82 | Fluoroquinolone, macrolide, penam | |
mdtF | 81 | Fluoroquinolone, macrolide, penam | |
mdtH | 84 | Fluoroquinolone | |
mdtK | 66 | Fluoroquinolone | |
mdtM | 83 | Nucleoside, lincosamide, fluoroquinolone, phenicol, disinfectant agents and antiseptics | |
mdtN | 85 | Nucleoside, disinfectant and antiseptics | |
mdtO | 82 | Nucleoside, disinfectant and antiseptics | |
mdtP | 83 | Nucleoside, disinfectant and antiseptics | |
msbA | 85 | Nitroimidazole | |
tolC | 85 | Peptide, aminoglycoside, tetracycline, aminocoumarin, penem, phenicol, fluoroquinolone, carbapem, macrolide, disinfecting agents and antiseptics, cephalosporin, glycylcycline, rifamycin, cephamycin | |
vgaC | 6 | Streptogramin, pleuromutilin, streptogramin A, lincosamide | |
Phosphonics | FosA7 | 4 | Phosphonic acid |
mdtG | 84 | Phosphonic acid | |
Sulfonamides | sul1 | 5 | Sulphonamide |
sul2 | 7 | Sulphonamide | |
sul3 | 1 | Sulphonamide | |
Tetracyclines | tet(A) | 2 | Tetracycline |
tet(C) | 6 | Tetracycline | |
tet(D) | 1 | Tetracycline | |
Trimethoprim-derivatives | dfrA12 | 4 | Diaminopyrimidine |
dfrA15 | 3 | Diaminopyrimidine |
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Onyeka, L.O.; Adesiyun, A.A.; Ismail, A.; Allam, M.; Keddy, K.H.; Thompson, P.N. Evidence for Horizontal Transmission and Recirculation of Shiga Toxin-Producing Escherichia coli in the Beef Production Chain in South Africa Using Whole Genome Sequencing. Pathogens 2024, 13, 732. https://doi.org/10.3390/pathogens13090732
Onyeka LO, Adesiyun AA, Ismail A, Allam M, Keddy KH, Thompson PN. Evidence for Horizontal Transmission and Recirculation of Shiga Toxin-Producing Escherichia coli in the Beef Production Chain in South Africa Using Whole Genome Sequencing. Pathogens. 2024; 13(9):732. https://doi.org/10.3390/pathogens13090732
Chicago/Turabian StyleOnyeka, Libby Obumneke, Abiodun A. Adesiyun, Arshad Ismail, Mushal Allam, Karen H. Keddy, and Peter N. Thompson. 2024. "Evidence for Horizontal Transmission and Recirculation of Shiga Toxin-Producing Escherichia coli in the Beef Production Chain in South Africa Using Whole Genome Sequencing" Pathogens 13, no. 9: 732. https://doi.org/10.3390/pathogens13090732