Advertisement

Current Microbiology

, Volume 76, Issue 12, pp 1407–1416 | Cite as

Antibiotic Resistance of LACTOBACILLUS Strains

  • Elizaveta A. Anisimova
  • Dina R. YarullinaEmail author
Article

Abstract

The study provides phenotypic and molecular analyses of the antibiotic resistance in 20 Lactobacillus strains including 11 strains newly isolated from fermented plant material. According to the results of disc diffusion method, 90% of tested lactobacilli demonstrated sensitivity to clindamycin and 95% of strains were susceptible to tetracycline, erythromycin, and rifampicin. Ampicillin and chloramphenicol were found to inhibit all bacteria used in this study. The vast majority of tested strains revealed phenotypic resistance to vancomycin, ciprofloxacin, and aminoglycosides. Most of Lactobacillus strains showed high minimum inhibitory concentrations (MICs) of cefotaxime, ceftriaxone, and cefazolin and therefore were considered resistant to cephalosporins. All the strains exhibited multidrug resistance. The occurrence of resistance genes was associated with phenotypic resistance, with the exception of phenotypically susceptible strains that contained genes for tetracycline (tetK, tetL) and erythromycin (ermB, mefA) resistance. The vanX gene for vancomycin resistance was among the most frequently identified among the lactobacilli (75% of strains), but the occurrence of the parC gene for ciprofloxacin resistance was sporadic (20% of strains). Our results mainly evidence the intrinsic nature of the resistance to aminoglycosides in lactobacilli, though genes for enzymatic modification of streptomycin aadA and aadE were found in 20% of tested strains. The occurrence of extended spectrum beta-lactamases (ESBL) was unknown in Lactobacillus, but our results revealed the blaTEM gene in 80% of strains, whereas blaSHV and blaOXA-1 genes were less frequent (20% and 15% of strains, respectively).

Notes

Acknowledgements

This work was supported by the program of competitive growth of Kazan Federal University, RFBR Grants No 18–34-00268 and 17–00-00456.

Author Contributions

EA designed the experiments, carried out the study, interpreted the data and drafted the manuscript. DY designed the study, supervised all experiments and reviewed the manuscript. All authors read and approved the final manuscript.

Compliance with Ethical Standards

Conflict of interests

The authors declare that there is no conflict of interests regarding the publication of this paper.

Ethical Approval

Ethical approval was not required.

Supplementary material

284_2019_1769_MOESM1_ESM.docx (31 kb)
Supplementary file1 (DOCX 31 kb)
284_2019_1769_MOESM2_ESM.tif (1.1 mb)
Supplementary file2 (TIFF 1119 kb)

References

  1. 1.
    Ammor MS, Flórez AB, Mayo B (2007) Antibiotic resistance in non-enterococcal lactic acid bacteria and bifidobacterial. Food Microbiol 24:559–570.  https://doi.org/10.1016/j.fm.2006.11.001 CrossRefPubMedGoogle Scholar
  2. 2.
    Ammor MS, Flórez AB, Van Hoek AHAM, de los Reyes-Gavilán CG, Aarts HJM, Margolles A, et al (2008) Molecular characterization of intrinsic and acquired antibiotic resistance in lactic acid bacteria and bifidobacteria. J Mol Microbiol Biotechnol 14:6–15.  https://doi.org/10.1159/000106077 CrossRefPubMedGoogle Scholar
  3. 3.
    Ammor MS, Gueimonde M, Danielsen M, Zagorec M, van Hoek AH, de Los Reyes-Gavilán CG, Mayo B, Margolles A (2008) Two different tetracycline resistance mechanisms, plasmid-carried tet(L) and chromosomally located transposon-associated tet(M), coexist in Lactobacillus sakei Rits 9. Appl Environ Microbiol 74(5):1394–1401.  https://doi.org/10.1128/AEM.01463-07 CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Anisimova E, Yarullina D (2018) Characterization of erythromycin and tetracycline resistance in Lactobacillus fermentum strains. Int J Microbiol.  https://doi.org/10.1155/2018/3912326 CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Anisimova EA, Yarullina DR, Ilinskaya ON (2017) Antagonistic activity of lactobacilli isolated from natural ecotopes. Microbiology 86(6):708–713.  https://doi.org/10.1134/S0026261717060054 CrossRefGoogle Scholar
  6. 6.
    Bernardeau M, Vernoux JP, Henri-Dubernet S, Guéguen M (2008) Safety assessment of dairy microorganisms: the Lactobacillus genus. Int J Food Microbiol 126:278–285.  https://doi.org/10.1016/j.ijfoodmicro.2007.08.015 CrossRefPubMedGoogle Scholar
  7. 7.
    Bruslik NL, Akhatova DR, Toimentseva AA, Abdulkhakov SR, Yarullina DR (2015) Estimation of probiotic lactobacilli drug resistance. J Antibiotics and Chemotherapy 60(3–4):6–13Google Scholar
  8. 8.
    Canton R, Coque TM (2006) The CTX-M beta-lactamase pandemic. Curr Opin Microbiol 9:466–475.  https://doi.org/10.1016/j.mib.2006.08.011 CrossRefPubMedGoogle Scholar
  9. 9.
    Charteris WP, Kelly PM, Morelli L, Collins JK (1998) Antibiotic susceptibility of potentially probiotic Lactobacillus species. J Food Protection 61(12):1636–1643CrossRefGoogle Scholar
  10. 10.
    Colom K, Perez J, Alonson R, Fernandez-Aranguiz A, Larino E, Cisterna R (2003) Simple and reliable multiplex PCR assay for detection of blaTEM, bla SHV and bla OXA-1 genes in Enterobacteriaceae. FEMS Microbiol Lett 223:147–151.  https://doi.org/10.1016/S0378-1097(03)00306-9 CrossRefPubMedGoogle Scholar
  11. 11.
    Danielsen M, Wind A (2003) Susceptibility of Lactobacillus spp. to antimicrobial agents. Int J Food Microbiol 82:1–11CrossRefGoogle Scholar
  12. 12.
    De Man JC, Rogosa M, Sharpe MT (1960) A medium for the cultivation of lactobacilli. J Appl Bacteriol 23:130–135CrossRefGoogle Scholar
  13. 13.
    Delcour J, Ferain T, Deghorain M, Palumbo E, Hols P (1999) The biosynthesis and functionality of the cell-wall of lactic acid bacteria. Antonie Van Leeuwenhoek 76:159–184CrossRefGoogle Scholar
  14. 14.
    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(12):3866–71. https://doi.org/doi:10.1128/AEM.00589-09 CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Duar RM, Lin XB, Zheng JZ, Martino ME, Grenier T, Pérez-Muñoz ME, Leulier F, Gänzle M, Walter J (2017) Lifestyles in transition: evolution and natural history of the genus Lactobacillus. FEMS Microbiol Rev 41:S27–S48.  https://doi.org/10.1093/femsre/fux030 CrossRefPubMedGoogle Scholar
  16. 16.
    Egervärn M, Roos S, Lindmark H (2009) Identification and characterization of antibiotic resistance genes in Lactobacillus reuteri and Lactobacillus plantarum. J Appl Microbiol 107(5):1658–1668.  https://doi.org/10.1111/j.1365-2672.2009.04352.x CrossRefPubMedGoogle Scholar
  17. 17.
    Faridi A, Kareshk AT, Fatahi-Bafghi M, Ziasistani M, Ghahraman MRK, Seyyed-Yousefi SZ, Shakeri N, Kalantar-Neyestanaki D (2018) Detection of methicillin-resistant Staphylococcus aureus (MRSA) in clinical samples of patients with external ocular infection. Iranian J Microbiol 10(4):215–219Google Scholar
  18. 18.
    Feld L, Schjorring S, Hammer K, Licht TR, Danielsen M, Krogfelt K, Wilcks A (2008) Selective pressure affects transfer and establishment of a Lactobacillus plantarum resistance plasmid in the gastrointestinal environment. J Antimicrob Chemother 61(4):845–852.  https://doi.org/10.1093/jac/dkn033 CrossRefPubMedGoogle Scholar
  19. 19.
    Fu KP, Neu HC (1978) Beta-lactamase stability of HR756, a novel cephalosporin compared to that of cefuroxime and cefoxitin. Antimicrob Agents Chemother 14(3):322–326.  https://doi.org/10.1128/aac.14.3.322 CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Fukao M, Tomita H, Yakabe T, Nomura T, Ike Y, Yajima N (2009) Assessment of antibiotic resistance in probiotic strain Lactobacillus brevis KB290. J Food Prot 72(9):1923–1929CrossRefGoogle Scholar
  21. 21.
    Gevers D, Danielsen M, Huys G, Swings J (2003) Molecular characterization of tet(M) genes in Lactobacillus isolates from different types of fermented dry sausage. Appl Environ Microbiol 69(2):1270–1275.  https://doi.org/10.1128/aem.69.2.1270-1275.2003 CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Gharajalar SN, Firouzamandi M (2017) Molecular detection of antibiotic resistance determinants in Lactobacillus bacteria isolated from human dental plaques. J Med Microbiol Infect Dis 5(3–4):51–55Google Scholar
  23. 23.
    Gueimonde M, Sánchez B, de Los Reyes-Gavilán CG, Margolles A (2013) Antibiotic resistance in probiotic bacteria. Front Microbiol 4:202.  https://doi.org/10.3389/fmicb.2013.00202 CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Guo H, Pan L, Li L, Lu J, Kwok L, Menghe B, Zhang H, Zhang W (2017) Characterization of antibiotic resistance genes from Lactobacillus isolated from traditional dairy products. J Food Sci 82(3):724–730.  https://doi.org/10.1111/1750-3841.13645 CrossRefPubMedGoogle Scholar
  25. 25.
    Han JH, Li XF, Gao WH, Walczak P, Zhang BL, Jia YM (2013) Susceptibility of Lactobacillus pentosus strains isolated from fermented products to streptomycin and kanamycin. International Food Research Journal 20(4):1927–1931Google Scholar
  26. 26.
    Handwerger S, Skoble J (1995) Identification of chromosomal mobile element conferring high-level vancomycin resistance in Enterococcus faecium. Antimicrob Agents Chemother 39(2446):2453Google Scholar
  27. 27.
    Hummel AS, Hertel C, Holzapfel WH, Franz CM (2007) Antibiotic resistances of starter and probiotic strains of lactic acid bacteria. Appl Environ Microbiol 73(3):730–739CrossRefGoogle Scholar
  28. 28.
    Ilinskaya ON, Ulyanova VV, Yarullina DR, Gataullin IG (2017) Secretome of intestinal bacilli: a natural guard against pathologies. Front Microbiol 8:1666.  https://doi.org/10.3389/fmicb.2017.01666 CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    James L, Beena AK, Anupa A, Sreeshma N (2016) Antibiogram of lactobacilli isolated from four different niches. J Microbiol Microb Technol 1(1):4Google Scholar
  30. 30.
    Jorgensen JH, Hindler JF, Reller LB, Weinstein MP (2007) New consensus guidelines from the Clinical and Laboratory Standards Institute for antimicrobial susceptibility testing of infrequently isolated or fastidious bacteria. Clin Infect Dis 44:280–286.  https://doi.org/10.1086/510431 CrossRefPubMedGoogle Scholar
  31. 31.
    Kastner S, Perreten V, Bleuler H, Hugenschmidt G, Lacroix C, Meile L (2006) Antibiotic susceptibility patterns and resistance genes of starter cultures and probiotic bacteria used in food. J Syst Appl Microbiol 29(2):145–155.  https://doi.org/10.1016/j.syapm.2005.07.009 CrossRefGoogle Scholar
  32. 32.
    Katla AK, Kruse H, Johnsen G, Herikstad H (2001) Antimicrobial susceptibility of starter culture bacteria used in Norwegian dairy products. Int J Food Microbiol 67(1–2):147–152CrossRefGoogle Scholar
  33. 33.
    Khan U, Afsana S, Kibtia M, Hossain M, Choudhury N, Ahsan CR (2019) Presence of blaCTX-M antibiotic resistance gene in Lactobacillus spp. isolated from Hirschsprung diseased infants with stoma. J Infect Dev Ctries 13(5):426–433. https://doi.org/10.3855/jidc.10968 CrossRefGoogle Scholar
  34. 34.
    Kirtzalidou E, Pramateftaki P, Kotsou M, Kyriacou A (2011) Screening for lactobacilli with probiotic properties in the infant gut microbiota. Anaerobe 17(6):440–443.  https://doi.org/10.1016/j.anaerobe.2011.05.007 CrossRefPubMedGoogle Scholar
  35. 35.
    Klein G, Hallman C, Casas IA, Abad J, Lowers J, Reuter G (2000) Exclusion of vanA, vanB and vanC type glycopeptide resistance in strains of Lactobacillus reuteri and Lactobacillus rhamnosus used as probiotics by polymerase chain reaction and hybridization methods. J Appl Microbiol 89(5):815–824CrossRefGoogle Scholar
  36. 36.
    Klein G, Pack A, Reuter G (1998) Antibiotic resistance patterns of enterococci and occurrence of vancomycin-resistant enterococci in raw minced beef and pork in Germany. Appl Environ Microbiol 64(5):1825–1830PubMedPubMedCentralGoogle Scholar
  37. 37.
    Korhonen JM, Danielsen M, Mayo B, Egervarn H, Axelsson L, Huys G et al (2008) Antimicrobial susceptibility and proposed microbiological cut-off values of lactobacilli by phenotypic determination. Int J Probiotics Prebiotics 3:257–268Google Scholar
  38. 38.
    Lahtinen SJ, Boyle RJ, Margolles A, Frías R, Gueimonde M (2009) Safety assessment of probiotics. In: Charalampopoulos D, Rastall RA (eds) Prebiotics and Probiotics Science and Technology. Springer-Verlag, Berlin, pp 1193–1225CrossRefGoogle Scholar
  39. 39.
    Li S, Li Z, Wei W, Ma C, Song X, He W, Tian J, Huo X (2015) Association of mutation patterns in GyrA and ParC genes with quinolone resistance levels in lactic acid bacteria. J Antibiot (Tokyo) 68(2):81–87.  https://doi.org/10.1038/ja.2014.113 CrossRefGoogle Scholar
  40. 40.
    Liu C, Zhang ZY, Dong K, Yuan JP, Guo XK (2009) Antibiotic resistance of probiotic strains of lactic acid bacteria isolated from marketed foods and drugs. Biomed Environ Sci 22(5):401–412.  https://doi.org/10.1016/S0895-3988(10)60018-9 CrossRefPubMedGoogle Scholar
  41. 41.
    Martel A, Meulenaere V, Devriese LA, Decostere A, Haesebrouck F (2003) Macrolide and lincosamide resistance in the gram-positive nasal and tonsillar flora of pigs. Microb Drug Resist 9(3):293–297.  https://doi.org/10.1089/107662903322286508 CrossRefPubMedGoogle Scholar
  42. 42.
    Mayrhofer S, van Hoeck AHAM, Mair C, Huys G, Arts HJM, Kneifel W et al (2010) Antibiotic susceptibility of members of the Lactobacillus acidophilus group using broth microdilution and molecular identification of their resistance determinants. Int J Food Microbiol 144(1):81–87.  https://doi.org/10.1016/j.ijfoodmicro.2010.08.024 CrossRefPubMedGoogle Scholar
  43. 43.
    Melo TA, Dos Santos TF, Pereira LR, Passos HM, Rezende RP, Romano CC (2017) Functional profile evaluation of Lactobacillus fermentum TCUESC01: A New Potential Probiotic Strain Isolated during Cocoa Fermentation. Biomed Res Int.  https://doi.org/10.1155/2017/5165916 CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Mendonça AA, de Lucena BT., de Morais MM., de Morais MA Jr (2016) First identification of Tn916-like element in industrial strains of Lactobacillus vini that spread the tet-M resistance gene. FEMS Microbiol Lett  https://doi.org/10.1093/femsle/fnv240 CrossRefPubMedGoogle Scholar
  45. 45.
    Moosdeen F (1997) The evoluation of resistance to cephalosporins. Clin Infect Dis 24(3):487–493.  https://doi.org/10.1093/clinids/24.3.487 CrossRefPubMedGoogle Scholar
  46. 46.
    Naas T, Cuzon G, Bogaerts P, Glupczynski Y, Nordmann P (2011) Evaluation of a DNA microarray (Check-MDR CT102) for the rapid detection of TEM, SHV and CTX-M extended-spectrum ß-lactamases (ESBLs), and of KPC, OXA-48, VIM, IMP, and NDM-1 carbapenemases. J Clin Microbiol 49(4):1608–1613. https://doi.org/doi:10.1128/JCM.02607-10 CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Nicoloff H, Bringel F (2003) ISLpl1 is a functional IS30-related insertion element in Lactobacillus plantarum that is also found in other lactic acid bacteria. Appl Environ Microbiol 69(10):6032–6040.  https://doi.org/10.1128/AEM.69.10.6032-6040.2003 CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    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(2):217–224.  https://doi.org/10.1016/j.ijfoodmicro.2007.11.018 CrossRefPubMedGoogle Scholar
  49. 49.
    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(1):73–76.  https://doi.org/10.1016/S0378-1097(03)00929-7 CrossRefPubMedGoogle Scholar
  50. 50.
    Rojo-Bezares B, Saenz 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(3):234–240.  https://doi.org/10.1016/j.ijfoodmicro.2006.06.007 CrossRefPubMedGoogle Scholar
  51. 51.
    Saarela M, Mättö J, Mattila-Sandholm T (2002) Safety aspects of Lactobacillus and Bifidobacterium species originating from human oro-gastrointestinal tract or from probiotic products. Microbial Ecology in Health and Disease 14(4):233–240.  https://doi.org/10.1080/08910600310002127 CrossRefGoogle Scholar
  52. 52.
    Sabouni F, Movahedi Z, Mahmoudi S, Pourakbari B, Valian SK, Mamishi S (2016) High frequency of vancomycin resistant Enterococcus faecalis in children: an alarming concern. Journal of preventive medicine and hygiene 57(4):E201–E204PubMedPubMedCentralGoogle Scholar
  53. 53.
    Salminen MK, Rautelin H, Tynkkynen S, Poussa T, Saxelin M, Valtonen V, Järvinen A (2006) Lactobacillus bacteremia, species identification, and antimicrobial susceptibility of 85 blood isolates. A Clin Infect Dis 42(5):e35–44.  https://doi.org/10.1086/500214 CrossRefPubMedGoogle Scholar
  54. 54.
    Sharma P, Tomar SK, Goswami P, Sangwan V, Singh R (2014) Antibiotic resistance among commercially available probiotics. Food Res Int 57:176–195.  https://doi.org/10.1016/j.foodres.2014.01.025 CrossRefGoogle Scholar
  55. 55.
    Sukmarini L, Mustopa AZ, Normawati M, Muzdalifah I (2014) Identification of antibiotic-resistance genes from lactic acid bacteria in indonesian fermented foods. HAYATI Journal of Biosciences 21:3:144–150 EISSN: 2086–4094. https://doi.org/10.4308/hjb.21.3.144 CrossRefGoogle Scholar
  56. 56.
    Thal L, Donabedian S, Robinson-Dunn B, Chow JW, Dembry L, Clewell DB, Alshab D, Zervos MJ (1998) Molecular analysis of glycopeptide-resistant Enterococcus faecium isolates collected from Michigan hospitals over a 6-year period. J Clinical Microbiol 36(11):3303–3308Google Scholar
  57. 57.
    van Hoek AHAM, Margolles A, Damig KJ, Korhonen JM, Zycka-Krzesinka J, Bardowsky JK et al (2008) Molecular assessment of erythromycin and tetracycline resistance genes in lactic acid bacteria and bifidobacteria and their relation to the phenotypic resistance. International Journal of Probiotics and Prebiotics 3(4):271–280Google Scholar
  58. 58.
    Werner G, Klare I, Witte W (1999) Large conjugative vanA plasmids in vancomycin-resistant Enterococcus faecium. J Clinical Microbiol 37(7):2383–2384Google Scholar
  59. 59.
    Werner G, Willems RJL, Hildebrandt B, Klare IW (2003) Witte Influence of transferable genetic determinants on the outcome of typing methods commonly used for Enterococcus faecium. J Clinical Microbiol 41(4):1499–1506.  https://doi.org/10.1128/JCM.41.4.1499-1506.2003 CrossRefGoogle Scholar
  60. 60.
    Zhou JS, Pillidge CJ, Gopal PK, Gill HS (2005) Antibiotic susceptibility profiles of new probiotic Lactobacillus and Bifidobacterium strains. Int J Food Microbiology 98(2):211–217.  https://doi.org/10.1016/j.ijfoodmicro.2004.05.011 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of MicrobiologyInstitute of Fundamental Medicine and Biology, Kazan Federal UniversityKazanRussian Federation

Personalised recommendations