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Antibiotic susceptibility and heterogeneity in technological traits of lactobacilli isolated from Algerian goat’s milk

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Abstract

The objective of this study was to identify and study the heterogeneity of technological traits of lactobacilli from goat’s milk of Algeria and to evaluate in vitro their safety aspect. Using API50 CHL system and 16S rDNA sequencing, 51 % of strains were assigned as Lactobacillus plantarum, 34 % as L. pentosus, 7 % as L. rhamnosus and 8 % as L. fermentum. A large variability was noted for the acidifying capacity in skim milk after 6, 12 and 24 h of incubation. All strains expressed aminopeptidase activity against alanine-ρ-NA and leucine-ρ-NA at different levels. All strains were resistant to vancomycin and most of strains showed more susceptibility to β-lactam antibiotic. High susceptibility toward the inhibitors of protein synthesis was also observed. Minimum inhibitory concentrations data obtained revealed that isolates were susceptible to penicillin and chloramphenicol, and resistant to gentamicin and vancomycin. Minimum inhibitory concentrations distribution of other antibiotics showed variability. The analysis of graphical representation of principal component analysis of technological properties of L. plantarum and L. pentosus strains showed diversity among the isolates. Finally, eight L. plantarum (LAM1, LAM3, LAM21, LAM25, LAM35, LF15, LAM34, and LAM35), four L. pentosus (LAM38, LAM39, LF9 and LF16) and two L. rhamnosus (LF3 and LF10) strains, could be good candidates as adjunct culture in dairy product in Algeria.

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References

  • Adams M, Mitchell R (2002) Fermentation and pathogen control: a risk assessment approach. Int J Food Microbiol 79:75–83

    Article  CAS  Google Scholar 

  • Altschul SF, Madden TL, Schäffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  Google Scholar 

  • Ammor MS, Flóre AB, Mayo B (2007) Antibiotic resistance in non-enterococcal lactic acid bacteria and bifidobacterium. Food Microbiol 24:559–570

    Article  CAS  Google Scholar 

  • Ayad EHE, Nashat S, El-Sadek N, Metwaly H, El-Soda M (2004) Selection of wild lactic acid bacteria isolated from traditional Egyptian dairy products according to production and technological criteria. Food Microbiol 21:715–725

    Article  Google Scholar 

  • Aymerich T, Martin B, Garriga M, Vidal-Carou MC, Bover-Cid S, Hugas M (2006) Safety properties and molecular strain typing of lactic acid bacteria from slightly fermented sausages. J Appl Microbiol 100:40–49

    Article  CAS  Google Scholar 

  • Badis A, Guetarni D, Moussa-Boudjemaa B, Henni DE, Tornadijo ME, Kihal M (2004a) Identification and technological properties oflactic acid bacteria isolated from raw goat milk of four Algerian races. Food Microbiol 21:343–349

    Article  CAS  Google Scholar 

  • Badis A, Guetarni D, Moussa-Boudjemaa B, Henni DE, Tornadijo ME, Kihal M (2004b) Identification and technological properties oflactic acid bacteria isolated from raw goat milk of four Algerian races. Food Microbiol 21:579–588

    Article  Google Scholar 

  • Belletti N, Gatti M, Bottari B, Neviani E, Tabanelli G, Gardini F (2009) Antibiotic resistance of Lactobacilli isolated from two Italian Hard Cheeses. J Food Prot 72:2162–2169

    CAS  Google Scholar 

  • Bernardeau M, Vernoux J, Henri-Dubernet S, Guéguen M (2008) Safety assessment of dairy microorganisms: the Lactobacillus genus. Int J Food Microbiol 126:278–285

    Article  CAS  Google Scholar 

  • Bertazzoni ME, Benini A, Marzotto M, Sbarbati A, Ruzzenente O, Ferrario R, Hendriks H, Dellaglio F (2004) Assessment of novel probiotic Lactobacillus casei strains for the production of functional dairy foods. Int Dairy J 14:723–736

    Article  Google Scholar 

  • Bude-Ugarte M, Guglielmotti D, Giraffa G, Reinheimer JA, Hynes E (2006) Nonstarter lactobacilli from Argentinean cheeses. J Food Prot 69:2983–2991

    Google Scholar 

  • Charteris WP, Kelly PM, Morelli L, Collins JK (1998) Antibiotic susceptibility of potentially probiotic Lactobacillus species. J Food Prot 61:1636–1643

    CAS  Google Scholar 

  • Christensen JE, Dudley EG, Pederson JA, Steele JL (1999) Peptidases and amino acid catabolism in lactic acid bacteria. Antonie Van Leeuwenhoek 76:217–246

    Article  CAS  Google Scholar 

  • Coeuret V, Dubernet S, Bernardeau M, Gueguen M, Vernoux JP (2003) Isolation, characterisation and identification of lactobacilli focusing mainly on cheeses and other dairy products. Lait 83:269–306

    Article  CAS  Google Scholar 

  • Coppola R, Succi M, Tremonte P, Reale A, Salzano G, Sorrentino E (2005) Antibiotic suscebtibility of Lactobacillus rhamnosus strains isolated from Parmigiano Reggiano cheese. Lait 85:193–204

    Article  CAS  Google Scholar 

  • Dagdemir E, Ozdemir S (2008) Technological characterization of the natural lactic acid bacteria of artisanal Turkish white pickled cheese. Int J Dairy Technol 61:133–140

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • De Vries MC, Vaughan EE, Kleerebezem M, de Vos WM (2006) Lactobacillus plantarum survival, functional and potential probiotic properties in the human intestinal tract. Int Dairy J 16:1018–1028

    Article  Google Scholar 

  • Delgado S, Flórez AB, Mayo B (2005) Antibiotic susceptibility of Lactobacillus and Bifidobacterium species from the human gastrointestinal tract. Curr Microbiol 50:202–207

    Article  CAS  Google Scholar 

  • Dunne C, O’Mahony L, Murphy L, Thornton G, Morrisey D, O’Halloran S, Feeney M, Flynn S, Fitzgerald G, Daly C, Kiely B, O’Sullivan GC, Shanahan F, Collins JK (2001) In vitro selection criteria for probiotic bacteria of human origin: correlation with in vivo findings. Am J Clin Nutr 73:386S–392S

    CAS  Google Scholar 

  • Elisha BG, Courvalin P (1995) Analysis of genes encoding dalanine: d-alanine ligase-related enzymes in Leuconostoc mesenteroides and Lactobacillus spp. Gene 152:79–83

    Article  CAS  Google Scholar 

  • European Food Safety Authority (EFSA) (2008) Scientific opinion of the panel on biological hazards on a request from the European food safety authority on food borne antimicrobial resistance as a biological hazard. EFSA J 765:1–87, SCAN

    Google Scholar 

  • Euzeby JP (1997) List of bacterial names with standing in nomenclature: a folder available on the internet(URL: http://www.bacterio.cict.fr/). Int J Syst Bacteriol 47:590–592

  • Flórez AB, Delgado S, Mayo B (2005) Antimicrobial susceptibility of lactic acid bacteria isolated from a cheese environment. Can J Microbiol 51:51–58

    Article  Google Scholar 

  • Gatti M, Contarini G, Naviani E (1999) Effectiveness of Chemometric techniques in discrimination of Lactobacillus helveticus biotypes from natural dairy starter cultures on the basis of phenotypic characteristics. Appl Environ Microbiol 65:1450–1454

    CAS  Google Scholar 

  • Giraffa G, Paris A, Valcavi L, Gatti M, Neviani E (2001) Genotypic and phenotypic heterogeneity of Streptococcus thermophilus strains isolated from dairy products. J Appl Microbiol 91:937–943

    Article  CAS  Google Scholar 

  • Giraffa G, Abdrighetto C, Antonello C, Gatti M, Lazzi C, Marcazzan G, Lombardi A, Neviani E (2004) Genotypic and phenotypic diversity of Lactobacillus delbrueckii subsp. lactis strains of dairy origin. Int J Food Microbiol 91:129–139

    Article  CAS  Google Scholar 

  • Halami PM, Chandrashekar A, Nand K (2000) Lactobacillus farciminis MD, a newer strain with potential for bacteriocin and antibiotic assay. Lett Appl Microbiol 30:197–202

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Jayne-Williams DJ (1976) The application of miniaturized methods for characterization of various organisms isolated from the animal gut. J Appl Microbiol 40:189–200

    CAS  Google Scholar 

  • Jenson MP, Ardö Y (2010) Variation in aminopeptidase and aminotransferase activities of six cheese related Lactobacillus helveticus strains. Int Dairy J 20:149–155

    Article  Google Scholar 

  • Kandler O, Weiss N (1986) Genus Lactobacillus Beijerinck 1901, 212 AL. In: Sneath PHA, Mair NS, Sharpe ME, Holt JG (eds) Bergey’s manual of systematic bacteriology, vol 2. Williams & Wilkins, Baltimore, pp 1209–1234

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Klein G, Pack A, Bonaparte C, Reuter G (1998) Taxonomy and physiology of probiotic lactic acid bacteria. Int J Food Microbiol 41:103–25

    Article  CAS  Google Scholar 

  • 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 89:815–24

    Article  CAS  Google Scholar 

  • Kotsou MG, Mitsou EK, Oikonomou IG, Kyriacou AA (2008) In vitro assessment of probiotic properties of Lactobacillus strains from infant gut microflora. Food Biotechnol 22:1–17

    Article  CAS  Google Scholar 

  • Leroy F, de Vuyst L (2004) Lactic acid bacteria as functional starter cultures for the food fermentation industry. Trends Food Sci Technol 15:67–78

    Article  CAS  Google Scholar 

  • Linaje R, Coloma MD, Pérez-Martinez G, Zúñiga M (2004) Characterization of faecal enterococci from rabbits for the selection of probiotic strains. J Appl Microbiol 96:761–771

    Article  CAS  Google Scholar 

  • Macedo AC, Viera M, Poças R, Malcata FX (2000) Peptide hydrolase system of lactic acid bacteria isolated from Serra da Estrela cheese. Int Dairy J 10:769–774

    Article  CAS  Google Scholar 

  • Malek R, El-Attar A, Mohamed M, Anwar S, El-Soda BC (2012) Technological and safety properties display biodiversity among enterococci isolated from two Egyptian cheeses, “Ras” and “Domiati”. Int J Food Microbiol 153:314–322

    Article  Google Scholar 

  • Maragkoudakis PA, Zoumpopoulou G, Miaris C, Kalantzopoulos G, Pot B, Tsakalidou E (2006) Probiotic potential of Lactobacillus strains isolated from dairy products. Int Dairy J 16:189–199

    Article  CAS  Google Scholar 

  • Marroki A, Zúñiga M, Kihal M, Pérez-Martínez G (2011) Characterization of Lactobacillus from Algerian goat’s milk based on phenotypic, 16S rDNA sequencing and their technological properties. Braz J Microbiol 42:158–171

    Article  CAS  Google Scholar 

  • Martin-Platero AM, Valdivia E, Maqueda M, Martinez-Bueno M (2007) Fast, convenient, and economical method for isolating genomic DNA from lactic acid bacteria using a modification of the protein “salting-out” procedure. Anal Biochem 366:102–104

    Article  CAS  Google Scholar 

  • Massart DL, Vandegiste BGM, Deming SN, Michotte Y, Kaufmann L (1988) Chemometrics: a textbook. Elsevier Science Publishers, Amsterdam

    Google Scholar 

  • Mathur S, Singh R (2005) Antibiotic resistance in food lactic acid bacteria—a review. Int J Food Microbiol 105:281–295

    Article  CAS  Google Scholar 

  • Mattila-Sandholm T, Mättö J, Saarela M (1999) Lactic acid bacteria with health claims-interactions and interference with gastrointestinal flora. Int Dairy J 9:25–35

    Article  Google Scholar 

  • Milesi MM, Vinderola G, Sabbag N, Meinardi CA, Hynes E (2009) Influenceon cheese proteolysis and sensory characteristics of non-starter lactobacilli strains with probiotic potential. Food Res Int 42:1186–1196

    Article  CAS  Google Scholar 

  • Monteagudo-Mera A, Rodriguez-Aparicio L, Rua J, Martinez-Blanco H, Navasa N, Garcia-Armesto MR, Ferrero MA (2012) In vitro evaluation of physiological probiotic properties of different lactic acid bacteria strains of dairy and human origin. J Funct Foods 4:5 3 1–5 4 1

    Article  CAS  Google Scholar 

  • Nieto-Arribas P, Poveda JM, Seseña S, Palop LI, Cabezas L (2009) Technological characterization of Lactobacillus isolates from traditional manchego cheese for potential use as adjunct starter cultures. Food Control 20:1092–1098

    Article  CAS  Google Scholar 

  • Pirainoa P, Zottaa T, Ricciardia A, McSweeneyb PLH, Parentea E (2008) Acid production, proteolysis, autolytic and inhibitory properties of lactic acid bacteria isolated from pasta filata cheeses: a multivariate screening study. Int Dairy J 18:81–92

    Article  Google Scholar 

  • Psono L, Kotzamanides C, Andrighetto C, Lombardi A, Tzanetakis N, Litopoulou-Tzanetaki E (2006) Genotypic and phenotypic heterogeneity in Enterococcus isolated from Batzos, a raw goat milk cheese. Int J Food Microbiol 109:109–120

    Article  Google Scholar 

  • Requena T, Pelaez C, Desmazeaud MJ (1991) Caracterization of lactococci and lactobacilli isolated from semi-hard goat’s cheese. J Dairy Res 58:137–145

    Article  Google Scholar 

  • Ross PR, Morgan S, Hill C (2002) Preservation and fermentation: past, present and future. Int J Food Microbiol 79:3–16

    Article  CAS  Google Scholar 

  • 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. Microb Ecol Health Dis 14:233–340

    CAS  Google Scholar 

  • Schillinger U, Lücke FK (1987) Identification of lactobacilli from meat and meat products. Food Microbiol 4:199–208

    Article  Google Scholar 

  • Settanni L, Moschetti G (2010) Non-starter lactic acid bacteria used to improve cheese quality and provide health benefits. Food Microbiol 27:691–697

    Article  CAS  Google Scholar 

  • Smulders FJM, Barendsen P, van Logtestijn JG, Mossel DAA, van Der Marel GM (1986) Lactic acid: consideration in favour of its acceptance as a meat decontaminant. J Food Technol 21:419–436

    Article  CAS  Google Scholar 

  • Stiles ME, Holzapfel WH (1997) Lactic acid bacteria of food and their current taxonomy. Int J Food Microbiol 36:1–29

    Article  CAS  Google Scholar 

  • Temmerman R, Pot B, Huys G, Swings J (2003) Identification and antibiotic susceptibility of bacterial isolates from probiotic products. Int J Food Microbiol 81:1–10

    Article  CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  Google Scholar 

  • Tynkkynen S, Singh KV, Varmanen P (1998) Vancomycin resistance factor of Lactobacillus rhamnosus GG in relation to enterococcal vancomycin resistance (van) genes. Int J Food Microbiol 41:195–204

    Article  CAS  Google Scholar 

  • Vandamme P, Pot B, Gillis M, De Vos P, Kersters K, Swings J (1996) Polyphasic taxonomy, a consensus approach to bacterial systematic. Microbiol Rev 60:407–438

    CAS  Google Scholar 

  • Vásques A, Molin G, Pettersson B, Antonsson M, Ahrné S (2005) DNA-based classification and sequence heterogeneities in the 16S rRNA genes of Lactobacillus casei/paracasei and related species. Syst Appl Microbiol 28:430–441

    Article  Google Scholar 

  • Veyrat A, Monedero V, Perez-Martinez G (1994) Glucose transport by the phosphoenolpyruvate:mannose phosphotransferase system in Lactobacillus casei ATCC 393 and its role in carbon catabolite repression. Microbiology 140:1141–1149

    Article  CAS  Google Scholar 

  • Vlkova E, Rada V, Popelarova P, Trojanova I, Killer J (2006) Antimicrobial susceptibility of Bifidobacteria isolated from gastrointestinal tract of calves. Livest Sci 105:253–259

    Article  Google Scholar 

  • Xanthopoulos V, Hatzikamari M, Adamidis T, Tzaneetakis N, Tsakalidou E, Litopoulou-Tzanetaki E (2000) Heterogeneity of Lactobacillus plantarum isolated from Feta cheese throughout ripening. J Appl Microbiol 88:1056–1064

    Article  CAS  Google Scholar 

  • Zarazaga M, Sainz Y, Portillo A, Tenorio C, Ruiz-Larrea RF, 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  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

    Article  CAS  Google Scholar 

  • Zotta T, Ricciardi A, Parente E (2007) Enzymatic activities of lactic acid bacteria isolated from Cornetto di Matera sourdoughs. Int J Food Microbiol 115:165–172

    Article  CAS  Google Scholar 

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Acknowledgments

Authors would like to expresses their gratitude to “Ministère de l’Enseignement Supérieur et de la Recherche Scientifique Algérien” and the Spanish Ministry of Science and Innovation for partially funded of this work. We are grateful to Dr Gaspar Perez Martinez (Director of laboratory of lactic acid bacteria and probiotic) - Instituto de Agroquímica y Tecnología de los Alimentos (IATA), Consejo Superior de Investigaciones Científicas (CSIC), Burjassot -Valencia- Espagne, for our acceptance in the laboratory and Dr Manuel Zúñiga for him excellent technical assistance and helpful.

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Bousmaha-Marroki, L., Marroki, A. Antibiotic susceptibility and heterogeneity in technological traits of lactobacilli isolated from Algerian goat’s milk. J Food Sci Technol 52, 4708–4723 (2015). https://doi.org/10.1007/s13197-014-1556-7

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