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Survey of antibiotic resistance traits in strains of Lactobacillus casei/paracasei/rhamnosus

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Abstract

In this study the occurrence of antibiotic resistance (AR) traits was evaluated in 184 lactic acid bacteria (LAB) strains belonging to the species Lactobacillus casei/paracasei/rhamnosus and isolated from various sources. The strains were tested for resistance at the cut-off values fixed by the European Food Safety Authority (EFSA) for the antibiotics ampicillin, chloramphenicol, clindamycin, gentamicin, erythromycin, kanamycin, streptomycin and tetracycline, in order to distinguish resistant from susceptible strains. The strains that were not inhibited at the cut-off concentrations for one or more antibiotics, namely 27 L. paracasei and 50 L. rhamnosus strains, were further examined for minimum inhibitory concentration (MIC) and presence of acquired genes encoding resistance to the specific antibiotics by PCR assays. A minority of these strains exhibited MIC values that indicated a potentially acquired AR for ampicillin (one L. paracasei strain), clindamycin (two L. paracasei and one L. rhamnosus strains), gentamicin (two L. rhamnosus strains) and tetracycline (two L. paracasei strains and one L. rhamnosus strain); however, the genetic determinants responsible for resistance could not be identified. This study highlighted a low frequency of AR phenotypes and the absence of the most frequently acquired AR genes in the L. casei/paracasei/rhamnosus strains examined, thus evidencing a low risk related to AR dissemination by these bacteria.

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References

  • Aminov RI, Garrigues-Jean JN, Mackie RJ (2001) Molecular ecology of tetracycline resistance: development and validation of primers for detection of tetracycline resistance genes encoding ribosomal protection proteins. Appl Environ Microbiol 67:22–32. doi:10.1128/AEM. 67.1.22-32.2001

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Aquilanti L, Garofalo C, Osimani A, Silvestri G, Vignaroli C, Clementi F (2007) Isolation and molecular characterization of antibiotic-resistant lactic acid bacteria from poultry and swine meat products. J Food Prot 70:557–565

    CAS  PubMed  Google Scholar 

  • Bartalesi F, Veloci S, Baragli F, Mantengoli E, Guidi S, Bartolesi AM, Mannino R, Pecile P, Bartoloni A (2012) Successful tigecycline lock therapy in a Lactobacillus rhamnosus catheter-related bloodstream infection. Infection 40:331–334. doi:10.1007/s15010-011-0196-3

    Article  CAS  PubMed  Google Scholar 

  • Briggiler-Marcó M, Capra ML, Quiberoni A, Vinderola G, Reinheimer JA, Hynes E (2007) Nonstarter Lactobacillus strains as adjunct cultures for cheese making: in vitro characterization and performance in two model cheeses. J Dairy Sci 90:4532–4542. doi:10.3168/jds.2007-0180

  • Cataloluk O, Gogebakan B (2004) Presence of drug resistance in intestinal lactobacilli of dairy and human origin in Turkey. FEMS Microbiol Lett 236:7–12. doi:10.1111/j.1574-6968.2004.tb09620.x

    Article  CAS  PubMed  Google Scholar 

  • Clementi F, Aquilanti L (2011) Recent investigations and updated criteria for the assessment of antibiotic resistance in food lactic acid bacteria. Anaerobe 17:394–398. doi:10.1016/j.anaerobe.2011.03.021

    Article  CAS  PubMed  Google Scholar 

  • Comunian R, Daga E, Dupré I, Paba A, Devirgiliis C, Piccioni V, Perozzi G, Zonenschain D, Rebecchi A, Morelli L, De Lorentiis A, Giraffa G (2010) Susceptibility to tetracycline and erythromycin of Lactobacillus paracasei strains isolated from traditional Italian fermented foods. Int J Food Microbiol 138:151–156. doi:10.1016/j.ijfoodmicro.2009.11.018

    Article  CAS  PubMed  Google Scholar 

  • Coppola R, Succi M, Sorrentino A, Iorizzo M, Grazia L (2003) Survey of lactic acid bacteria during the ripening of Caciocavallo cheese produced in Molise. Lait 83:211–222

    Article  CAS  Google Scholar 

  • Danielsen M, Wind A (2003) Susceptibility of Lactobacillus spp. to antimicrobial agents. Int J Food Microbiol 82:1–11. doi:10.1016/S0168-1605(02)00254-4

    Article  CAS  PubMed  Google Scholar 

  • Delgado S, Florez AB, Mayo B (2005) Antibiotic susceptibility of Lactobacillus and Bifidobacterium species from the human gastrointestinal tract. Curr Microbiol 50:202–207. doi:10.1007/s00284-004-4431-3

    Article  CAS  PubMed  Google Scholar 

  • Devirgiliis C, Coppola D, Barile S, Colonna B, Perozzi G (2009) Characterization of the Tn916 conjugative transposon in a food-borne strain of Lactobacillus paracasei. Appl Environ Microbiol 75:3866–3871. doi:10.1128/AEM. 00589-09

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Douillard FP, Kant R, Ritari J, Paulin L, Palva A, de Vos WM (2013) Comparative genome analysis of Lactobacillus casei strains isolated from Actimel and Yakult products reveals marked similarities and points to a common origin. Microb Biotechnol 6:576–587. doi:10.1111/1751-7915.12062

    Article  PubMed Central  PubMed  Google Scholar 

  • Dušková M, Karpíšková R (2013) Antimicrobial resistance of lactobacilli isolated from food. Czech J Food Sci 31:27–32

    Google Scholar 

  • EFSA-European Food Safety Authority (2011) Approaches to risk assessment in the area of antimicrobial resistance, with an emphasis on commensal microorganisms. EFSA J 9:196–224

    Google Scholar 

  • EFSA-European Food Safety Authority (2012) Guidance on the assessment of bacterial susceptibility to antimicrobials of human and veterinary importance. EFSA Panel on Additives and Products or Substances used in Animal Feed (FEEDAP). EFSA J 10:2740–2749

    Google Scholar 

  • EFSA-European Food Safety Authority (2013) Scientific opinion on the maintenance of the list of QPS biological agents intentionally added to food and feed (2013 update). EFSA panel on biological hazards (BIOHAZ). EFSA J 11(11):3449–3557

    Google Scholar 

  • Egervärn M, Roos S, Lindmark H (2009) Identification and characterization of antibiotic resistance genes in Lactobacillus reuteri and Lactobacillus plantarum. J Appl Microbiol 107:1658–1668. doi:10.1111/j.1365-2672.2009.04352.x

    Article  PubMed  Google Scholar 

  • Flórez AB, Alegría A, Rossi F, Delgado S, Felis GE, Torriani S, Mayo B (2014) Molecular identification and quantification of tetracycline and erythromycin resistance genes in spanish and italian retail cheeses. Biomed Res Int 2014:746859. doi:10.1155/2014/746859

    Article  PubMed Central  Google Scholar 

  • Garofalo C, Vignaroli C, Zandri G, Aquilanti L, Bordoni D, Osimani A, Clementi F, Biavasco F (2007) Direct detection of antibiotic resistance genes in specimens of chicken and pork meat. Int J Food Microbiol 113:75–83. doi:10.1016/j.ijfoodmicro.2006.07.015

    Article  CAS  PubMed  Google Scholar 

  • Gupta A, Mann B, Kumar R, Sangwan RB (2013) ACE-inhibitory activity of cheddar cheeses made with adjunct cultures at different stages of ripening. Adv Dairy Res 1:102. doi:10.4172/2329-888X.1000102

    Google Scholar 

  • Hummel A, Holzapfel WH, Franz CM (2007) Characterisation and transfer of antibiotic resistance genes from enterococci isolated from food. Syst Appl Microbiol 30:1–7. doi:10.1016/j.syapm.2006.02.004

    Article  CAS  PubMed  Google Scholar 

  • Huys G, D’Haene K, Danielsen M, Mättö J, Egervärn M, Vandamme P (2008) Phenotypic and molecular assessment of antimicrobial resistance in Lactobacillus paracasei strains of food origin. J Food Prot 71:339–344

    CAS  PubMed  Google Scholar 

  • Iacumin L, Ginaldi F, Manzano M, Anastasi V, Reale A, Zotta T, Rossi F, Coppola R, Comi G (2015) High resolution melting analysis (HRM) as a new tool for the identification of species belonging to the Lactobacillus casei group and comparison with species-specific PCRs and multiplex PCR. Food Microbiol 46:357–367. doi:10.1016/j.fm.2014.08.007

    Article  CAS  PubMed  Google Scholar 

  • Ishihara K, Nakajima K, Kishimoto S, Atarashi F, Muramatsu Y, Hotta A, Ishii S, Takeda Y, Kikuchi M, Tamura Y (2013) Distribution of antimicrobial-resistant lactic acid bacteria in natural cheese in Japan. Microbiol Immunol 57:684–691. doi:10.1111/1348-0421.12090

    Article  CAS  PubMed  Google Scholar 

  • Jacobsen CN, Rosenfeldt Nielsen V, Hayford AE, Møller PL, Michaelsen KF, Paerregaard A, Sandström B, Tvede M, Jakobsen M (1999) Screening of probiotic activities of forty-seven strains of Lactobacillus spp. by in vitro techniques and evaluation of the colonization ability of five selected strains in humans. Appl Environ Microbiol 65:4949–4956. doi: 0099-2240/99/$04.0010

  • Jensen LB, Frimodt-Møller N, Aarestrup FM (1999) Presence of erm gene classes in gram-positive bacteria of animal and human origin in Denmark. FEMS Microbiol Lett 170:151–158. doi:10.1111/j.1574-6968.1999.tb13368.x

    Article  CAS  PubMed  Google Scholar 

  • Klare I, Konstabel C, Müller-Bertling S, Reissbrodt R, Huys G, Vancanneyt M, Swings J, Goossens H, Witte W (2005) Evaluation of new broth media for microdilution antibiotic susceptibility testing of lactobacilli, pediococci, lactococci, and bifidobacteria. Appl Environ Microbiol 71:8982–8986. doi:10.1128/AEM. 71.12.8982-8986.2005

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Klare I, Konstable C, Werner G, Huys G, Vankerchoven V, Kahlmeter G, Hildebrandt B, Müller-Bertling S, Witte W, Goossens H (2007) Antimicrobial susceptibilities of Lactobacillus, Pediococcus and Lactococcus human isolates and cultures intended for probiotic or nutritional use. J Antimicrob Chemoth 59:900–912. doi:10.1093/jac/dkm035

    Article  CAS  Google Scholar 

  • Korhonen JM, Van Hoek AH, Saarela M, Huys G, Tosi L, Mayrhofer S, Wright AV (2010) Antimicrobial susceptibility of Lactobacillus rhamnosus. Benef Microbes 1:75–80. doi:10.3920/BM2009.0002

    Article  CAS  PubMed  Google Scholar 

  • Lin CF, Fung ZF, Wu CL, Chung TC (1996) Molecular characterization of a plasmid-borne (pTC82) chloramphenicol resistance determinant (cat-TC) from Lactobacillus reuteri G4. Plasmid 36:116–124. doi:10.1006/plas.1996.0039

    Article  CAS  PubMed  Google Scholar 

  • Ng LK, Martin I, Alfa M, Mulvey M (2001) Multiplex PCR for the detection of tetracycline resistant genes. Mol Cell Probes 15:209–215. doi:10.1006/mcpr.2001.0363

    Article  CAS  PubMed  Google Scholar 

  • Ouoba LI, Lei V, Jensen LB (2008) Resistance of potential probiotic lactic acid bacteria and bifidobacteria of African and European origin to antimicrobials: determination and transferability of the resistance genes to other bacteria. Int J Food Microbiol 121:217–224. doi:10.1016/j.ijfoodmicro.2007.11.018

    Article  CAS  PubMed  Google Scholar 

  • Reale A, Di Renzo T, Succi M, Tremonte P, Coppola R, Sorrentino E (2011) Identification of lactobacilli isolated in traditional ripe wheat sourdoughs by using molecular methods. World J Microbiol Biotechnol 27:237–244

    Article  Google Scholar 

  • Reale A, Di Renzo T, Rossi F, Zotta T, Preziuso M, Iacumin L, Parente E, Sorrentino E, Coppola R (2015) Tolerance of Lactobacillus casei, Lactobacillus paracasei and Lactobacillus rhamnosus strains to stress factors encountered in food processing and in gastro-intestinaltract. LWT Food Sci Technol (2014). doi:10.1016/j.lwt.2014.10.022

    Google Scholar 

  • Rojo-Bezares B, Sáenz Y, Poeta P, Zarazaga M, Ruiz-Larrea F, Torres C (2006) Assessment of antibiotic susceptibility within lactic acid bacteria strains isolated from wine. Int J Food Microbiol 111:234–240. doi:10.1016/j.ijfoodmicro.2006.06.007

    Article  CAS  PubMed  Google Scholar 

  • Rosander A, Connolly E, Roos S (2008) Removal of antibiotic resistance gene-carrying plasmids from Lactobacillus reuteri ATCC 55730 and characterization of the resulting daughter strain, L. reuteri DSM 17938. Appl Environ Microbiol 74:6032–6040. doi:10.1128/AEM. 00991-08

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rossi F, Dellaglio F, Torriani S (2006) Evaluation of recA gene as a phylogenetic marker in the classification of dairy propionibacteria. Syst Appl Microbiol 29:463–469. doi:10.1016/j.syapm.2006.01.001

    Article  CAS  PubMed  Google Scholar 

  • Rossi F, Gatto V, Sabattini G, Torriani S (2012) An assessment of factors characterising the microbiology of Grana Trentino cheese, a Grana-type cheese. Int J Dairy Technol 65:404–409. doi:10.1111/j.1471-0307.2012.00844.x

    Article  Google Scholar 

  • Sutcliffe J, Grebe T, Tait-Kamradt A, Wondrack L (1996) Detection of erythromycin-resistant determinants by PCR. Antimicrob Agents Chemother 40:2562–2566. doi: 0066-4804/96/$04.0010

  • Tannock GW, Luchansky JB, Miller L, Connell H, Thode-Andersen S, Mercer AA, Klaenhammer TR (1994) Molecular characterization of a plasmid-borne (pGT633) erythromycin resistance determinant (ermGT) from Lactobacillus reuteri 100–63. Plasmid 31:60–71. doi:10.1006/plas.1994.1007

    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. doi:10.1016/j.resmic.2009.12.010

    Article  CAS  PubMed  Google Scholar 

  • Villedieu A, Diaz-Torres ML, Hunt N, McNab R, Spratt DA, Wilson M, Mullany P (2003) Prevalence of tetracycline resistance genes in oral bacteria. Antimicrob Agents Chemother 47:878–882. doi:10.1128/AAC. 47.3.878-882.2003

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ya T, Zhang Q, Chu F, Merritt J, Bilige M, Sun T, Du R, Zhang H (2008) Immunological evaluation of Lactobacillus casei Zhang: a newly isolated strain from koumiss in Inner Mongolia, China. BMC Immunol 9:68. doi:10.1186/1471-2172-9-68

    Article  PubMed Central  PubMed  Google Scholar 

  • Zhou JS, Pillidge CJ, Gopal PK, Gill HS (2005) Antibiotic susceptibility profiles of new probiotic Lactobacillus and Bifidobacterium strains. Int J Food Microbiol 98:211–217. doi:10.1016/j.ijfoodmicro.2004.05.011

    Article  CAS  PubMed  Google Scholar 

  • Zonenschain D, Rebecchi A, Morelli L (2009) Erythromycin- and tetracycline-resistant lactobacilli in Italian fermented dry sausages. J Appl Microbiol 107:1559–1568. doi:10.1111/j.1365-2672.2009.04338.x

    Article  CAS  PubMed  Google Scholar 

  • Zotta T, Ricciardi A, Ianniello RG, Parente E, Reale A, Rossi F, Iacumin L, Comi G, Coppola R (2014) Assessment of aerobic and respiratory growth in the Lactobacillus casei group. PLoS One 9:e99189. doi:10.1371/journal.pone.0099189

    Article  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

This study was carried out in the frame of the Future in Basic Research project “Genetic and physiological bases of aerobical metabolism in Lactobacillus rhamnosus and L. paracasei: fundamental and applied aspects”, code RBFR107V_002, Italian Ministry of Research and Instruction (MIUR).

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Authors and Affiliations

  1. Agriculture, Environment and Food Department (DIAAA), University of Molise, via De Sanctis, 86100, Campobasso, Italy

    Franca Rossi & Raffaele Coppola

  2. Institute of Food Science (ISA), National Research Council, via Roma 64, 83100, Avellino, Italy

    Tiziana Di Renzo, Marco Preziuso, Teresa Zotta, Raffaele Coppola & Anna Reale

  3. Department of Food Science, University of Udine, via Sondrio 2/A, 33100, Udine, Italy

    Lucilla Iacumin

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  1. Franca Rossi
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  2. Tiziana Di Renzo
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  3. Marco Preziuso
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  4. Teresa Zotta
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  6. Raffaele Coppola
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  7. Anna Reale
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Correspondence to Anna Reale.

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Rossi, F., Di Renzo, T., Preziuso, M. et al. Survey of antibiotic resistance traits in strains of Lactobacillus casei/paracasei/rhamnosus . Ann Microbiol 65, 1763–1769 (2015). https://doi.org/10.1007/s13213-014-1015-8

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  • DOI: https://doi.org/10.1007/s13213-014-1015-8

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