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. 2022 Dec 15;13(4):469–474. doi: 10.30466/vrf.2021.138938.3090

Genotypic and phenotypic tetracycline-based properties of Trueperella pyogenes isolates from bovine samples

Ozlem Şahan Yapicier 1,*, Dilek Ozturk 2, Mehmet Kaya 2
PMCID: PMC9840790  PMID: 36686870

Abstract

The purpose of this study was to investigate the tetracycline resistance in Trueperella pyogenes isolates from bovine samples in Burdur, Turkiye, and assess 16 tetracycline-resistance genes distribution among the isolates. Forty-nine T. pyogenes isolates were phenotypically characterized for anti-microbial resistance to doxycycline, oxytetracycline and tetracycline by disc diffusion method. Presence of tetracycline genes of T. pyogenes was investigated by multiplex and singleplex polymerase chain reaction. Our results indicated that 87.80% and 42.86% of the isolates were resistant to tetracycline and oxytetracycline, respectively, and the rate of resistance to doxycycline was 6.12%. Total of 21 (42.85%) were carrying tetracycline-resistance genes and tet(A) was present in 12 (24.49%) isolates; whereas, the tet(W) gene was identified in 9 (18.37%) and 2 (4.08%) of the isolates carried both tet(A) and tet(W), respectively. The study indicated antibiotic resistance patterns of tetracycline agents and links to the tet-genes among T. pyogenes were detected. It makes it worthwhile that this is the first report for detection of tet(A) gene in T. pyogenes.

Key Words: Cattle, Mastitis, Tetracycline resistance genes, Trueperella pyogenes

Introduction

Trueperella pyogenes (formerly Arcanobacterium pyogenes) most frequently occurs as a commensal and opportunistic pathogen of the gastrointestinal system as well as upper respiratory and urogenital tracts mucosae of domestic and wild animals.1,2 The T. pyogenes is a common causative agent of mastitis, metritis, abscesses, pneumonia, arthritis, endocarditis and osteomyelitis.3-7 Moreover, recent decreases in milk production being associated with mastitis, as well as causing reproductive losses and reductions in meat quality have increased interest in understanding the effects of pathogenic T. pyogenes.8,9 Among humans, sporadic cases of T. pyogenes infections have been reported in patients who have been in contact with animals.10-12

Traditional antibiotics such as beta-lactams have been administered for a long time in veterinary medicine to treat T. pyogenes.9,13 These situations can be often explained by the fact that there is limited information about the in vitro susceptibility of T. pyogenes against anti-microbials.13

Tetracyclines are used so extensively in veterinary medicine, providing broad-spectrum agents acting against a wide range of Gram -positive and -negative bacteria.14-16 However, several studies have reported that T. pyogenes is resistant to tetracyclines3,4,17-22 and tetracycline resistance is due to the acquisition of new genes, often associated with mobile elements.14,15 Especially, the tet(W) gene is thought to play an important role in tetracycline resistance; while, few studies have examined the distribution of tetracycline resistance genes (TCRs) in T. pyogenes.23

The main objective of this study was to determine the susceptibility of T. pyogenes to tetracycline-based anti-biotics agents and identify TCRs.

Materials and Methods

Bacterial strains. Forty-nine individual T. pyogenes strains cattle milk (n = 27) and calf synovial fluid (n = 22) obtained from Department of Microbiology, Faculty of Veterinary Medicine, Mehmet Akif Ersoy University, Burdur, Turkiye, 24 were investigated. The reference strain ATCC 19411 was used as a positive control for each examination.

Anti-microbial susceptibility. Resistance profiles of 49 T. pyogenes strains were determined on Mueller–Hinton agar (Oxoid, Basingstoke, UK) supplemented with 5.00% sheep blood using the Kirby-Bauer disk diffusion method according to the Clinical and Laboratory Standards Institute (CLSI) protocols.25 The following three tetracyclines (Oxoid) being commonly used in veterinary medicine were selected: Doxcyciline (30.00 μg), oxytetracycline (30.00 μg) and tetracycline (30.00 μg). Not all anti-microbial agents breakpoints are available for the determination of antibiotic susceptibility by disc diffusion test for T. pyogenes in CLSI. 25 Thus, the method used in this study was adapted from ones being described for other fastidious Gram-positive organisms.25 Then, the results were evaluated as antibiotic susceptible, intermediately susceptible and antibiotic resistant.

Primers. Primer pairs specific for 16 TCRs are listed in Table 1.26-38

Table 1.

Tetracycline resistance specific primers

Genes Primer sequence 5'-3' Amplicon size (bp)
tet (A) GCT ACA TCC TGC TTG CCT TC
CAT AGA TCG CCG TGA AGA GG		 210
tet (B) TTG GTT AGG GGC AAG TTT TG
GTA ATG GGC CAA TAA CAC CG		 659
tet (C) CTT GAG AGC CTT CAA CCC AG
ATG GTC GTC ATC TAC CTG CC		 418
tet (D) AAA CCA TTA CGG CAT TCT GC
GAC CGG ATA CAC CAT CCA TC		 787
tet(E) AAA CCA CAT CCT CCA TAC GC
AAA TAG GCC ACA ACC GTC AG		 278
tet(G) GCT CGG TGG TAT CTC TGC TC
AGC AAC AGA ATC GGG AAC AC		 468
tet(G) CAG CTT TCG GAT TCT TAC GG
GAT TGG TGA GGC TCG TTA GC		 844
tet(K) TCG ATA GGA ACA GCA GTA
CAG
CAG ATC CTA CTC CTT
		 169
tet(L) TCG TTA GCG TGC TGT CAT TC
GTA TCC CAC CAA TGT AGC CG		 267
tet(M) GTG GAC AAA GGT ACA ACG AG
CGG TAA AGT TCG TCA CAC AC		 406
tet(O) AAC TTA GGC ATT CTG GCT CAC
TCC CAC TGT TCC ATA TCG TCA		 515
tet(S) CAT AGA CAA GCC GTT GAC C
ATG TTT TTG GAA CGC CAG AG		 667
tet(P) CTT GGA TTG CGG AAG AAG AG
ATA TGC CCA TTT AAC CAC GC		 676
tet(Q) TTA TAC TTC CTC CGG CAT CG
ATC GGT TCG AGA ATG TCC AC		 904
tet(X) CAA TAA TTG GTG GTG GAC CC
TTC TTA CCT TGG ACA TCC CG		 468
tet(W) GACAACGAGAACGGACACTATG
CGCAATAGCCAGCAATGAACGC		 1,843
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DNA extraction. DNA extractions from T. pyogenes isolates were performed according to the instructions of the GeneJET Genomic DNA Purification Kit (Thermo Scientific, Waltham, USA). The DNAs were stored for use as template DNA at – 20.00 ˚C until amplification.

Polymerase chain reaction (PCR) conditions. Singeleplex PCR assay was carried out for tet(W) gene. The protocol was as follows: 25.00 µL reaction volumes containing 3.00 µL MgCl (25.00 mM, Thermo Fisher Scientific Baltics, Vinius, Lithuania), 0.50 µL dNTP (10.00 mM, Thermo Fisher Scientific Baltics), 10.00 pmols of primers and 0.20 µL Taq polymerase (5.00 U µL-1, Thermo Fisher Scientific Baltics) were used and PCR amplifications were performed with the following cycling conditions: 3 min at 94.00 ˚C, followed by 30 cycles of 1 min at 94.00 ˚C (denaturation) and 1 min at 54.00 ˚C (primer annealing), 1 min at 72.00 ˚C (extension) and 7 min at 72.00 ˚C (final extension). Multiplex PCR was performed for Tcrs and these genes were grouped as follows: Group I: tet(B), tet(C) and tet(D), Group II: tet(A), tet(E) and tet(G), Group III: tet(K), tet(L), tet(M), tet(O) and tet(S) and Group IV: tetA(P), tet(Q) and tet(X) as described by Ng et al. Each multiplexed group's PCR reaction mix concentration and amplification conditions were carried out following the previous report.39

Results

Antibiotic resistance. As shown in Table 2, 3/49 (6.12%) of the isolates were susceptible to all tetracyclines. Moreover, 43 (87.80%) and 21 (42.86%) of the isolates were resistant to oxytetracycline and tetracycline, respectively, and three isolates were resistant to doxycycline (6.12%). In addition, 7/32 (2.00%) and 9/32 (1.00%) of the isolates were resistant to two and three types of tetracyclines, respectively. Of the strains, 6/32 (18.80%) were resistant to all three tested anti-microbial agents (Fig. 1).

Table 2.

Anti-microbial susceptibility results of 49 Trueperella pyogenes isolates. Data are presented as number of isolates (%).

Anti-microbials Sensitive Intermediate Resistant
Doxycycline 43 (87.80) 3 (6.12) 3 (6.12)
Tetracycline 8 (16.32) 20 (40.81) 21 (42.86)
Oxytetracycline 3 (6.12) 3 (6.12) 43 (87.80)
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Fig. 1.

Fig. 1

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Kirby-Bauer disc diffusion susceptibility test on Trueperella pyogenes Mueller-Hinton agar supplemented with 5.00% sheep blood with A) doxycycline (30.00 μg), B) tetracycline (30.00 μg) and C) oxytetracycline (30.00 μg)

Antibiotic resistance genes distribution. Of the 49 T. pyogenes isolates, 21 (42.85%) carrying TCRs were identified; 12 (24.49%) with tet(A) and 9 (18.37%) with tet(W) are presented in Figure 2. In addition, 2 (4.08%) were found to carry both tet(A) and tet(W) genes. The tet(A) gene was identified in 11 (91.75%) isolates resistant to doxycycline, 9 (75.00%) isolates resistant to tetracycline and 1 (8.33%) isolate resistant to oxytetracycline. Moreover, 9 (100%) of the isolates resistant to oxytetracycline and 3 (33.33%) of the isolates resistant to tetracycline were found to possess the tet(W) gene. Both tet(A) and tet(W) genes exhibited 100% resistance against tetracycline and oxytetracycline; but none were resistant to doxycycline (Table 3).

Fig. 2.

Fig. 2

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Multiplex (A and B) and singleplex (C and D) PCR assay being performed using group II (tet(A), tet(E) and tet(G)) and tet(G) primers. A) M: 100 bp marker; Lanes 12, 19 and 20: tet(A) positive PCR products; Lanes 1-11,13-18 and 21-24: Negative; Lane 25: Negative control. B) M: 100 bp marker; Lanes 1-3: tet(A) positive PCR products; Lanes 4-6 and 8-10: Negative; Lane 7: Negative control. C) M: 100 bp marker; Lanes 4-7: tet(W) positive PCR products; Lanes 2 and 3: Negative; Lane 1: Negative control. D) M: 100 bp marker; Lanes 13, 17, 19, 24 and 25: tet(W) positive PCR products; Lanes 1-12,14-16,18 and 20-23: Negative; Lane 24: Negative control

Table 3.

Correlations between tet(A) and tet(W) genes with tetracyclines agents. Data are presented as number of isolates (%).

Anti-microbials tet A tet W tet both
Sensitive Intermediate Resistant Sensitive Intermediate Resistant Sensitive Intermediate Resistant
Doxycycline 10 (83.33) 1 (8.33) 1 (8.33) 9 (100) - - 2 (100) - -
Tetracycline 1 (8.33) 2 (16.70) 9 (75.00) - 6 (66.70) 3 (33.33) - - 2 (100)
Oxytetracycline 1 (8.33) - 11 (91.70) - - 9 (100) - - 2 (100)
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Discussion

Tetracyclines, including tetracycline, doxycycline, chlortetracycline, oxytetracycline and minocycline are commonly used for the treatment of bacterial infections in livestock animals.40-42 It is well accepted that tetracycline resistance causes resistance to other antibiotics.43 The purpose of this study was to investigate phenotypic and genotypic tetracycline resistance among the 49 T. pyogenes isolates. The highest anti-microbial resistance patterns were observed in 43 (87.80%) isolates, and 21 (42.86%) of the isolates were resistant to oxytetracycline and tetracycline. In addition, 87.80% were susceptible to doxycyciline, being excepted based on previous findings.44 The high levels of tetracycline3,4,17,20,45 and oxytetracycline resistance18,46,47 were similar with the previous studies.23 In contrast, Ribeiro et al., have reported T. pyogenes isolates being sensitive to tetracycline.5

In this study, singleplex and multiplex PCR assays were used to detect TCRs in T. pyogenes isolates. To the best of our knowledge, this is the first report examining the prevalence of these genes in T. pyogenes isolates in Turkiye. Here, we used four multiplex PCR groups to detect 15 TCRs (tet(A), (B), (C), (D), (E), (G), (H), (K), (L), (M), (O), (P), (Q), (S) and (X)) and singleplex PCR to detect the tet (W) gene. It is thought to reveal the screening of the tet(A) and tet(W) genes in this study which are associated with efflux and/or ribosomal protection mechanisms. This is the first report to identify the tet(A) gene in T. pyogenes isolates. Although the tet(A) gene has also been reported to be a common tet resistance gene in Gram-negative genera48, it is notable that, in this study, the tet(A) genes were found among the Gram-positive bacteria. Not suprisingly, the tet(W) gene is the fourth most common TCR based on previous studies.1,3,25,48,49 The predominant hypothesis for the presence of the tet(W) in commensal bacteria, such as T. pyogenes, is thought to be due to the acquisition from the ruminal wall of animals.1

As mentioned above, the tet(A) gene was found in 11(91.75%), 9(75.00%) and 1(8.33%) isolates being resistant to doxycycline, tetracycline and oxytetracycline, respectively. Also, 9 (100%) and 3 (33.33%) isolates being resistant to oxytetracycline and tetracycline possessed the tet(W) gene, respectively. In this study, the prevalence of tetracycline resistance due to the tet(A) gene was greater than the tet(W) gene, which is in contrast with findings from previous studies.1,23,49 According to Zhang et al., the tet(W) gene may confer antibiotic resistance, particularly multi-drug resistance; but, since three tetracycline preparations were used in this study, these findings were not confirmed.23 The presence of tet(A) and tet(W) genes exhibited 100% resistance against tetracycline and oxytetracycline; but, not doxycycline. Further, the lack of resistance genes in some resistant samples could have been due to the indefinite phenotypic resistance, lack of gene expression or other resistance mechanisms.43

The present study provides an overview of susceptibility to commonly used tetracycline preparations and the distribution of TCRs among T. pyogenes isolates. The findings in this study are important, since tetracycline resistance remains a significant concern and will contribute to the selection of effective anti-microbial agents against this pathogen in veterinary medicine. This is the first report of the tet(A) gene being present in T. pyogenes; while, the detection of tet(W) confirms its common presence in various bacterial isolates as reported previously. In addition to treatment, control measures should be chosen and improved depending on the type of T. pyogenes infection.

Conflict of interest

The authors declare that they have no competing interests.

Acknowledgments

Not applicable.

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