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Characterization of quinolone resistance mechanisms in lactic acid bacteria isolated from yogurts in China

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Abstract

Twenty-five strains of ciprofloxacin-resistant lactic acid bacteria (LAB; 14 Lactobacillus spp. and 11 Streptococcus thermophiles spp.) isolated from commercial yogurts in China were analyzed in this study. For each of these strains, amino acid changes associated with quinolone resistance-determining regions (QRDRs) were investigated using PCR-based detection methods. The same methodology was used to identify the presence of plasmid-mediated quinolone resistance (PMQR) genes in LAB. Sequencing analyses and an efflux pump inhibition test (using reserpine) were also performed as part of the analysis. Our results showed that typical mutations corresponding to quinolone resistance were found in the QRDRs of LAB strains. Detected mutations included Ser80Leu in parC, and Ser83Leu and Glu87Asp in gyrA. In addition, a Tyr74Phe substitution in parC, which had not previously been reported to be associated with quinolone resistance, was observed in two Lactobacillus delbrueckii subsp. bulgaricus strains. For each of the tested strains, the presence of the efflux pump inhibitor, reserpine, resulted in a two- to eightfold reduction in the minimum inhibitory concentrations (MICs) of ciprofloxacin. However, PMQR genes were not observed in any of the strains analyzed. Our results suggest that mutations in the QRDRs or efflux pump could be involved in ciprofloxacin resistance, and that a combination of these mechanisms may lead to increased ciprofloxacin resistance in LAB strains.

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References

  • Arioli S, Elli M, Ricci G, Mora D (2013) Assessment of the susceptibility of lactic acid bacteria to biocides. Int J Food Microbiol 163:1–5

    Article  CAS  PubMed  Google Scholar 

  • Betanzos-Cabrera G, Juárez-Verdayes MA, González-González G, Cancino-Díaz ME, Cancino-Díaz JC (2009) Gatifloxacin, moxifloxacin, balofloxacin resistance due to mutations in the gyrA and parC genes of Staphylococcus epidermidis strains isolated from patients with endophthalmitis, corneal ulcers and conjunctivitis. Ophthalmic Res 42:43–48

    Article  CAS  PubMed  Google Scholar 

  • Bourdichon F, Casaregola S, Forrokh C, Frisva JC, Gerds ML, Hammes WP, Harnett J, Huys G, Laulund S, Ouwehand A, Powell IB, Prajapati JB, Seto Y, Schure ET, Van Boven A, Vankerckhoven V, Zgoda A, Tuijtelaars S, Hansen EB (2012) Food fermentations: microorganisms with technological beneficial use. Int J Food Microbiol 154:87–97

    Article  CAS  PubMed  Google Scholar 

  • Cattoir V, Poirel L, Aubert C, Soussy CJ, Nordmann P (2008) Unexpected occurrence of plasmid-mediated quinolone resistance determinants in environmental Aeromonas spp. Emerg Infect Dis 14:231–237

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cavaco LM, Hasman H, Xia S, Aarestrup FM (2009) qnrD, a novel gene conferring transferable quinolone resistance in Salmonella enterica serovar Kentucky and Bovis morbificans strains of human origin. Antimicrob Agents Chemother 53:603–608

    Article  CAS  PubMed  Google Scholar 

  • Chen CR, Malik M, Snyder M, Drlica K (1996) DNA gyrase and topoisomerase IV on the bacterial chromosome: quinolone-induced DNA cleavage. J Mol Biol 258:627–637

    Article  CAS  PubMed  Google Scholar 

  • D’Aimmo MR, Modesto M, Biavati B (2007) Antibiotic resistance of lactic acid bacteria and Bifidobacterium spp. isolated from dairy and pharmaceutical products. Int J Food Microbiol 115:35–42

    Article  PubMed  Google Scholar 

  • Danielsen M, Wind A (2003) Susceptibility of Lactobacillus spp. to antimicrobial agents. Int J Food Microbiol 82:1–11

    Article  CAS  PubMed  Google Scholar 

  • Davies D (2003) Understanding biofilm resistance to antibacterial agents. Nat Rev Drug Discov 2:114–122

    Article  CAS  PubMed  Google Scholar 

  • European Commission (2001) Opinion of the Scientific Committee on Animal Nutrition on the criteria for assessing the safety of micro-organisms resistant to antibiotics of human clinical and veterinary importance. Accessed Jan. 24, 2003. http://ec.europa.eu/food/fs/sc/scan/out108_en.pdf

  • Frempong-Manso E, Raygada JL, DeMarco CE, Seo SM, Kaatz GW (2009) Inability of a reserpine-based screen to identify strains overexpressing efflux pump genes in clinical isolates of Staphylococcus aureus. Int J Antimicrob Agents 33:360–363

    Article  CAS  PubMed  Google Scholar 

  • Garvey MI, Piddock LJ (2008) The efflux pump inhibitor reserpine selects multidrug-resistant Streptococcus pneumoniae strains that overexpress the ABC transporters PatA and PatB. Antimicrob Agents Chemother 52:1677–1685

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Godreuil S, Galimand M, Gerbaud G, Jacquet C, Courvalin P (2003) Efflux pump Lde is associated with fluoroquinolone resistance in Listeria monocytogenes. Antimicrob Agents Chemother 47:704–708

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grkovic S, Brown MH, Skurray RA (2002) Regulation of bacterial drug export systems. Microbiol Mol Biol Rev 66:671–701

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hernández A, Sánchez MB, Martínez JL (2011) Quinolone resistance: much more than predicated. Front Microbiol 2:22

    Article  PubMed  PubMed Central  Google Scholar 

  • Hooper DC (1999) Mechanisms of fluoroquinolone resistance. Drug Resist Update 2:38–55

    Article  CAS  Google Scholar 

  • Hummel AS, Hertel C, Holzaptel WH, Franz CMAP (2007) Antibiotic resistances of starter and probiotic strains of lactic acid bacteria. Appl Environ Microbiol 73:730–739

    Article  CAS  PubMed  Google Scholar 

  • Ito H, Yoshida H, Bogaki-Shonai M, Niga T, Hattori H, Nakamura S (1994) Quinolone resistance mutations in the DNA gyrase gyrA and gyrB genes of Staphylococcus aureus. Antimicrob Agents Chemother 38:2014–2023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jacobsen L, Wilcks A, Hammer K, Huys G, Gevers D, Andersen SR (2007) Horizontal transfer of tet(M) and erm(B) resistance plasmids from food strains of Lactobacillus plantarum to Enterococcus faecalis JH2–2 in the gastrointestinal tract of gnotobiotic rats. FEMS Microbiol Ecol 59:158–166

    Article  CAS  PubMed  Google Scholar 

  • Jacoby GA (2005) Mechanisms of resistance to quinolones. Clin Infect Dis 41:S120–S126

    Article  CAS  PubMed  Google Scholar 

  • Jiang X, Zhou L, Gao D, Wang Y, Wang D, Zhang Z, Chen M, Su Y, Li L, Yan H, Shi L (2012) Expression of efflux pump gene lde in ciprofloxacin-resistant foodborne isolates of Listeria monocytogenes. Microbiol Immunol 56:843–846

    Article  CAS  PubMed  Google Scholar 

  • Jiang X, Yu T, Wu N, Meng H, Shi L (2014a) Detection of qnr, aac(6')-Ib-cr and qepA genes in Escherichia coli isolated from cooked meat products in Henan, China. Int J Food Microbiol 187:22–25

    Article  CAS  PubMed  Google Scholar 

  • Jiang X, Yu T, Jiang X, Zhang W, Zhang L, Ma J (2014b) Emergence of plasmid-mediated quinolone resistance genes in clinical isolates of Acinetobacter baumannii and Pseudomonas aeruginosa in Henan, China. Diagn Microbiol Infect Dis 79:381–383

    Article  CAS  PubMed  Google Scholar 

  • Jiang Y, Zhou Z, Qian Y, Wei Z, Yu Y, Hu S, Li L (2008) Plasmid-mediated quinolone resistance determinants qnr and aac(6’)-Ib-cr in extended-spectrum β-lactamase-producing Escherichia coli and Klebsiella pneumoniae in China. J Antimicrob Chemother 61:1003–1006

    Article  CAS  PubMed  Google Scholar 

  • Katla A-K, Kruse H, Johnsen G, Herikstad H (2001) Antimicrobial susceptibility of starter culture bacteria used in Norwegian dairy products. Int J Food Microbiol 67:147–152

    Article  CAS  PubMed  Google Scholar 

  • Kim K, Park J, Kwak H, Woo G (2011) Characterization of the quinolone resistance mechanism in foodborne Salmonella isolates with high nalidixic acid resistance. Int J Food Microbiol 146:52–56

    Article  CAS  PubMed  Google Scholar 

  • Klaenhammer TR, Barrangou R, Buck BL, Azcarate-Peril MA, Altermann E (2005) Genomic features of lactic acid bacteria effecting bioprocessing and health. FEMS Microbiol Rev 29:393–409

    Article  CAS  PubMed  Google Scholar 

  • Klare I, Konstabel C, Müller-Bertling S, Reissbrodt R, Huys G, Vancanneyt M, Swings J, Goossens H (2005) Evaluation of new broth media for microdilution antibiotic susceptibility testing of Lactobacilli, Pediococci, Lactococci, and Bifidobacteria. Appl Environ Microbiol 71:8982–8986

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li X, Nikaido H (2009) Efflux-mediated drug resistance in bacteria: an update. Drugs 69:1555–1623

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martínez-Martínez L, Pascual A, Jacoby GA (1998) Quinolone resistance from a transferable plasmid. Lancet 351:797–799

    Article  PubMed  Google Scholar 

  • Martins M, Mccusker M, Amaral L, Fanning S (2011) Mechanisms of antibiotic resistance in Salmonella: efflux pumps, genetics, quorum sensing and biofilm formation. Lett. Drug Des Discov 8:114–123

    Article  CAS  Google Scholar 

  • Masuda N, Sakagawa E, Ohya S, Gotoh N, Tsujimoto H, Nishino T (2000) Substrate specificities of MexAB-OprM, MexCD-OprJ, and MexXY-OprM efflux pumps in Pseudomonas aeruginosa. Antimicrob Agents Chemother 44:3322–3327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moreno C, Romero J, Espejo RT (2002) Polymorphism in repeated 16S rRNA genes is a common property of type strains and environmental isolates of the genus Vibrio. Microbiology 148:1233–1239

    Article  CAS  PubMed  Google Scholar 

  • Muñoz R, de la Campa AG (1996) ParC subunit of DNA topoisomerase IV of Streptococcus pneumoniae is a primary target of fluoroquinolones and cooperates with DNA gyrase A subunit in forming resistance phenotype. Antimicrob Agents Chemother 40:2252–2257

    PubMed  PubMed Central  Google Scholar 

  • Nawaz M, Wang J, Zhou A, Ma C, Wu X, Moore JE, Millar BC, Xu J (2011) Characterization and transfer of antibiotic resistance in lactic acid bacteria from fermented food products. Curr Microbiol 62:1081–1089

    Article  CAS  PubMed  Google Scholar 

  • Neyfakh AA, Borsch CM, Kaatz GW (1993) Fluoroquinolone resistance protein NorA of Staphylococcus aureus is a multidrug efflux transporter. Antimicrob Agents Chemother 37:128–129

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Noquchi N, Okada H, Narur K, Sasatsu M (2004) Comparison of the nucleotide sequence and expression of norA genes and microbial susceptibility in 21 strains of Staphylococcus aureus. Microb Drug Resist 10:197–203

    Article  Google Scholar 

  • Onodera Y, Okuda J, Tanaka M, Sato K (2002) Inhibitory activities of quinolones against DNA gyrase and topoisomerase IV of Enterococcus faecalis. Antimicrob Agents Chemother 46:1800–1804

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Petersen A, Jensen LB (2004) Analysis of gyrA and parC mutations in enterococci from environmental samples with reduced susceptibility to ciprofloxacin. FEMS Microbiol Lett 231:73–76

    Article  CAS  PubMed  Google Scholar 

  • Poirel L, Cattoir V, Nordmann P (2012) Plasmid-mediated quinolone resistance; interactions between human, animal, and environmental ecologies. Front Microbiol 3:24

    Article  PubMed  PubMed Central  Google Scholar 

  • Rodriquez-Alonso P, Femández-Otero C, Centeno JA, Garabal JI (2009) Antibiotic resistance in lactic acid bacteria and Micrococcaceae/Staphylococcaceae isolates from artisanal raw milk cheeses, and potential implications on cheese making. J Food Sci 74:M284–M293

    Article  Google Scholar 

  • Stavri M, Piddock LJ, Gibbons S (2007) Bacterial efflux pump inhibitors from natural sources. J Antimicrob Chemother 59:1247–1260

    Article  CAS  PubMed  Google Scholar 

  • Tanaka M, Wang T, Onodera Y, Uchida Y, Sato K (2000) Mechanism of quinolone resistance in Staphylococcus aureus. J Infect Chemother 6:131–139

    Article  CAS  PubMed  Google Scholar 

  • Toomey N, Bolton D, Fanning S (2010) Characterisation and transferability of antibiotic resistance genes from lactic acid bacteria isolated from Irish pork and beef abattoirs. Res Microbiol 161:127–135

    Article  CAS  PubMed  Google Scholar 

  • Wang M, Tran JH, Jacoby GA, Zhang Y, Wang F, Hooper DC (2003) Plasmid-mediated quinolone resistance in clinical isolates of Escherichia coli from Shanghai, China. Antimicrob Agents Chemother 47:2242–2248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang M, Guo Q, Xu X, Wang X, Ye X, Wu S, Hooper DC, Wang M (2009) New plasmid-mediated quinolone resistance gene, qnrC, found in a clinical isolate of Proteus mirabilis. Antimicrob Agents Chemother 53:1892–1897

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xia J, He L, Chen J (2011) Expression level of MexAB-OprM in multi-drug resistant Pseudomonas aeruginosa. Chin J Nosocomiol 21:221–223 (in Chinese)

    CAS  Google Scholar 

  • Zarazaga M, Sáenz Y, Portillo A, Tenorio C, Ruiz-Larrea F, Del Campo R, Baquero F, Torres C (1999) In vitro activities of ketolide HMR3647, macrolides, and other antibiotics against Lactobacillus, Leuconostoc, and Pediococcus isolates. Antimicrob Agents Chemother 43:3039–3041

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang H, Xie L, Zhang W, Zhou W, Su J, Liu J (2013) The association of biofilm formation with antibiotic resistance in lactic acid bacteria from fermented foods. J Food Safety 33:114–120

    Article  Google Scholar 

  • Zhou N, Zhang JX, Fan MT, Wang J, Guo G, Wei XY (2012) Antibiotic resistance of lactic acid bacteria isolated from Chinese yogurts. J Dairy Sci 95:4775–4783

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the Key Project of Natural Science of the Education Department of Henan Province, China (15A180006), the Key Scientific and Technological Project of Xinxiang (ZG15007), the Youth Science Foundation of Henan Normal University, and the Doctoral Scientific Research Foundation of Henan Normal University.

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Authors and Affiliations

  1. College of Life Sciences, Henan Normal University, Xinxiang, 453007, China

    Xiaobing Jiang, Shengdong Ji & Chune Zhou

  2. College of Life Science and Technology, Xinxiang University, Xinxiang, 453000, Peoples Republic of China

    Tao Yu & Xuannian Wang

  3. College of Life Science and Technology, Tongji University, Shanghai, 200092, China

    Danlei Zhou

  4. College of Light Industry and Food Sciences, South China University of Technology, Guangzhou, 510640, China

    Lei Shi

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  1. Xiaobing Jiang
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  2. Tao Yu
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Correspondence to Tao Yu.

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Jiang, X., Yu, T., Zhou, D. et al. Characterization of quinolone resistance mechanisms in lactic acid bacteria isolated from yogurts in China. Ann Microbiol 66, 1249–1256 (2016). https://doi.org/10.1007/s13213-016-1214-6

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  • DOI: https://doi.org/10.1007/s13213-016-1214-6

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