Serotypes, Antibiotic Susceptibility, Genotypic Virulence Profiles and SpaA Variants of Erysipelothrix rhusiopathiae Strains Isolated from Pigs in Poland
Abstract
:1. Introduction
2. Materials and Methods
2.1. Isolation of Erysipelothrix rhusiopathiae Strains
2.2. Identification of E. rhusiopathiae Strains
2.3. Serotyping of E. rhusiopathiae Strains
2.4. Antimicrobial Susceptibility Testing
2.5. Isolation of DNA
2.6. Detection of Resistance Genes
2.7. Sequence Analysis of the gyrA Gene
2.8. Detection of Virulence Genes
2.9. Whole spaA gene Amplification and Sequence Analysis
3. Results
3.1. Identification of E. rhusiopathiae Isolates
3.2. Serotyping
3.3. Antibiotic Susceptibility
3.4. Genotypic Resistance Profiles
3.5. Virulence-Associated Genes
3.6. SpaA Sequence Analysis
4. Discussion
4.1. Occurrence of E. rhusiopathiae Infections in Pigs
4.2. Serotypes of E. rhusiopathiae Strains
4.3. Antibiotic Susceptibility and Genotypic Resistance Profiles
4.4. Virulence Genes
4.5. SpaA Variants
4.6. Limitations of the Study
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Antimicrobial Agent | Breakpoints | Reference | ||
---|---|---|---|---|
S | I | R | ||
Ampicillin | ≤0.25 | – | – | CLSI VET06 [26] |
Ceftiofur | ≤2 | 4 | ≥8 | CLSI VET06 [26] |
Erythromycin | ≤0.25 | 0.5 | ≥1 | CLSI VET06 [26] |
Tylosin | ≤0.25 | 0.5 | ≥1 | CLSI VET06 breakpoints for erythromycin were adopted [26]. |
Clindamycin | ≤0.25 | 0.5 | ≥1 | CLSI VET06 [26] |
Lincomycin | ≤2 | 4–8 | ≥16 | CA-SFM/EUCAST breakpoints for Staphylococcus spp. were adopted [27] |
Tiamulin | ≤16 | – | ≥32 | Breakpoints were proposed based on MIC distribution and the presence of the lsaE gene |
Enrofloxacin | ≤0.5 | 1 | ≥2 | CLSI VET06 [26] |
Tetracycline | ≤4 | 8 | ≥16 | CLSI breakpoints for Staphylococcus spp. were adopted [25]; a breakpoint of ≥16 µg/mL has also been previously proposed for E. rhusiopathiae by other authors [1,28] |
Florfenicol | ≤8 | 16 | ≥32 | Chloramphenicol cut-offs recommended by CLSI [25] for Staphylococcus spp. and Enterobacteriaceae have been adopted |
Strain ID | Ser. | AMP | CEF | TET | ERY | TYL | LIN | CLI | TIA | ENR | FLO | STR | SPE | GEN | KAN | NEO | TR | TR/S | RIF | Resistance Genes |
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
ATCC 19414 | 2 | ≤0.06 | ≤0.06 | 0.5 | 0.25 | 0.125 | 0.5 | ≤0.06 | 4 | ≤0.25 | 2 | 128 | 64 | >512 | >512 | >512 | >512 | >512 | >128 | aadK |
1S | N | ≤0.06 | ≤0.06 | 1 | 0.125 | 0.125 | 1 | ≤0.06 | 2 | ≤0.25 | 4 | 32 | 32 | >512 | >512 | >512 | >512 | >512 | >128 | aadK |
2S | 6 | ≤0.06 | ≤0.06 | 0.5 | 0.125 | ≤0.06 | 0.5 | ≤0.06 | 2 | ≤0.25 | 2 | 64 | 16 | >512 | >512 | >512 | >512 | >512 | >128 | aadK |
3S | 1b | 0.125 | ≤0.06 | 32 | 0.25 | 0.125 | 0.5 | ≤0.06 | 4 | 16 | 4 | 128 | 32 | >512 | >512 | >512 | >512 | >512 | >128 | aadK, tetM, int-Tn |
4S | 1b | 0.125 | ≤0.06 | 64 | 0.5 | 0.125 | 0.5 | ≤0.06 | 4 | 16 | 4 | 256 | 128 | >512 | >512 | >512 | >512 | >512 | >128 | aadK, tetM, int-Tn |
5S | 2 | 0.125 | ≤0.06 | 32 | 0.25 | 0.125 | 1 | ≤0.06 | 4 | ≤0.25 | 4 | 256 | 64 | >512 | >512 | >512 | >512 | >512 | >128 | aadK, tetM, int-Tn |
6S | 5 | 0.125 | ≤0.06 | 32 | 0.25 | 0.125 | 0.5 | 0.25 | 2 | 8 | 4 | 32 | 64 | >512 | >512 | >512 | >512 | >512 | >128 | aadK, tetM, int-Tn |
7S | 1b | 0.125 | ≤0.06 | 32 | 0.25 | 0.125 | 0.5 | ≤0.06 | 2 | 16 | 2 | 256 | 128 | >512 | >512 | >512 | >512 | >512 | >128 | aadK, tetM, int-Tn |
8S | 8 | 0.125 | ≤0.06 | 32 | 0.25 | 0.25 | >64 | 2 | >128 | 16 | 4 | 128 | 64 | >512 | >512 | >512 | >512 | >512 | >128 | aadK, tetM, int-Tn, lnuB, lsaE |
9S | 2 | ≤0.06 | ≤0.06 | 32 | ≤0.06 | 0.25 | 0.5 | ≤0.06 | 4 | ≤0.25 | 2 | 256 | 32 | >512 | >512 | >512 | >512 | >512 | >128 | aadK, tetM, int-Tn |
10S | 5 | ≤0.06 | ≤0.06 | 64 | 0.25 | 0.125 | 0.5 | ≤0.06 | 4 | 8 | 2 | 256 | 32 | >512 | >512 | >512 | >512 | >512 | >128 | aadK, tetM, int-Tn |
11S | 1b | 0.25 | ≤0.06 | 64 | 0.25 | 0.125 | 0.5 | ≤0.06 | 4 | 16 | 2 | 128 | 64 | >512 | >512 | >512 | >512 | >512 | >128 | aadK, tetM, int-Tn |
12S | 1b | ≤0.06 | ≤0.06 | 0.125 | 0.25 | 0.125 | 0.5 | ≤0.06 | 4 | ≤0.25 | 4 | 32 | 64 | >512 | >512 | >512 | >512 | >512 | >128 | aadK |
13S | 1b | 0.125 | ≤0.06 | 64 | 0.125 | 0.125 | 0.5 | ≤0.06 | 4 | 16 | 2 | 128 | 32 | >512 | >512 | >512 | >512 | >512 | >128 | aadK, tetM, int-Tn |
14S | 2 | ≤0.06 | ≤0.06 | 0.5 | ≤0.06 | ≤0.06 | 0.125 | ≤0.06 | 1 | ≤0.25 | 4 | 32 | 32 | >512 | >512 | >512 | >512 | >512 | >128 | aadK |
Number and % of resistant strains | 0 | 0 | 10 71.4% | 0 | 0 | 1 7.1% | 1 7.1% | 1 7.1% | 8 57.1% | 0 | NA | NA | NA | NA | NA | NA | NA | NA |
Isolate | Serotype | Enrofloxacin MIC [µg/mL] | Antibiotic Susceptibility | Mutation at Position 257 of the gyrA Gene and Corresponding Change in aa Sequence | GenBank Accesion NUMER |
---|---|---|---|---|---|
ATCC 19414 | 2 | ≤0.25 | S | Thr86 (ACA) | LR134439.1 |
1S | N | ≤0.25 | S | Thr86 (ACA) | OP921301 |
2S | 6 | ≤0.25 | S | Thr86 (ACA) | OP921302 |
3S | 1b | 16 | R | Thr86→Ile (ACA→ATA) | OP921303 |
8S | 8 | 16 | R | Thr86→Ile (ACA→ATA) | OP921304 |
10S | 5 | 8 | R | Thr86→Lys (ACA→AAA) | OP921305 |
Gene/Locus Tag Acc. No. AP012027.1 | Gene Product/Predicted Function | Gene Prevalence |
---|---|---|
spa; ERH_0094 | Surface protection antigen A/adhesion to host cells | 100% |
spaB | Surface protection antigen B | 0% |
spaC | Surface protection antigen C | 0% |
nanH.1; ERH_0299 | Neuraminidase/spreading factor | 100% |
nanH.2; ERH-0761 | Neuraminidase/spreading factor | 100% |
cpsA; ERH_0157 | Capsule polysaccharide synthesis gene (glycosyl transferase)/resistance to complement | 100% |
ERH_1356 | ABC transporter metal-binding lipoprotein/adhesion of host cells | 100% |
intl; ERH_1472 | Internalin/invasion of epithelial cells | 100% |
rspA; ERH_0668 | Rhusiopathiae surface protein/biofilm formation | 100% |
rspB; ERH_0669 | Rhusiopathiae surface protein/biofilm formation | 100% |
algI; ERH_0402 | Alginate-O-acetyltransferase/resistance to phagocytosis | 100% |
sub; ERH_0260 | Cell-envelope associated proteinase, subtilase family | 100% |
hlyA; ERH_0150 | Hyaluronidase/adhesion-promoting factor | 100% |
fbpA; ERH_1034 | Fibronectin-binding protein/adhesion | 100% |
hlyIII; ERH_0649 | Haemolysin/lytic activity on red blood cells | 100% |
SpaA Variant | Serotype | Amino Acid (aa) Position | Number of C-Terminal Tandem Repeats | |||||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
38 | 54 | 55 | 70 | 101 | 109 | 139 | 178 | 195 | 232 | 257 | 303 | 423 | 426 | 435 | ||||
R32E11 vaccine strain | 2 | CCA (Pro) | GGG (Gly) | ATA (Ile) | AAT (Asn) | AAC (Asn) | CAT (His) | CAG (Gln) | GAT (Asp) | AAT (Asn) | ATC (Ile) | ATT (Ile) | GAG (Glu) | CCA (Pro) | AAA (Lys) | CCA (Pro) | 13 | |
Fujisawa type strain | 1a | GTA (Val) | AAA (Lys) | AAT (Asn) | GGT (Gly) | GAT (Asp) | CTT (Leu) | GGG (Gly) | GAA (Glu) | CTA (Leu) | 9 | |||||||
ATCC 19414 type strain | 2 | AAT (Asn) | 9 | |||||||||||||||
1 | 14S | 2 | AAT (Asn) | 9 | ||||||||||||||
2 | 1S | N | CAA (Gln) | AAT (Asn) | 9 | |||||||||||||
3 | 2S | 6 | GTA (Val) | AAA (Lys) | AAT (Asn) | GGT (Gly) | GAT (Asp) | GGG (Gly) | 9 | |||||||||
4 | 8S | 8 | GCG (Ala) | GTA (Val) | AAA (Lys) | AGC (Ser) | AAT (Asn) | GGT (Gly) | GAT (Asp) | GGG (Gly) | 7 | |||||||
5 | 12S | 1b | GTA (Val) | AAA (Lys) | AGC (Ser) | AAT (Asn) | AAG (Lys) | GGT (Gly) | GAT (Asp) | ACC (Thr) | GGG (Gly) | 8 | ||||||
6 | 3S, 4S, 6S, 7S, 10S, 11S, 13S | 1b, 5 | GTA (Val) | AAA (Lys) | AGC (Ser) | AAT (Asn) | GGT (Gly) | GAT (Asp) | GGG (Gly) | 8 or 9 | ||||||||
7 | 5S, 9S | 2 | GTA (Val) | AAA (Lys) | AGC (Ser) | AAT (Asn) | GGT (Gly) | GAT (Asp) | GGG (Gly) | CAA (Gln) | 9 |
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Dec, M.; Łagowski, D.; Nowak, T.; Pietras-Ożga, D.; Herman, K. Serotypes, Antibiotic Susceptibility, Genotypic Virulence Profiles and SpaA Variants of Erysipelothrix rhusiopathiae Strains Isolated from Pigs in Poland. Pathogens 2023, 12, 409. https://doi.org/10.3390/pathogens12030409
Dec M, Łagowski D, Nowak T, Pietras-Ożga D, Herman K. Serotypes, Antibiotic Susceptibility, Genotypic Virulence Profiles and SpaA Variants of Erysipelothrix rhusiopathiae Strains Isolated from Pigs in Poland. Pathogens. 2023; 12(3):409. https://doi.org/10.3390/pathogens12030409
Chicago/Turabian StyleDec, Marta, Dominik Łagowski, Tomasz Nowak, Dorota Pietras-Ożga, and Klaudia Herman. 2023. "Serotypes, Antibiotic Susceptibility, Genotypic Virulence Profiles and SpaA Variants of Erysipelothrix rhusiopathiae Strains Isolated from Pigs in Poland" Pathogens 12, no. 3: 409. https://doi.org/10.3390/pathogens12030409