Skip to main content
Log in

Probiotic characteristics and in vitro compatibility of a combination of Bifidobacterium breve M-16 V, Bifidobacterium longum subsp. infantis M-63 and Bifidobacterium longum subsp. longum BB536

  • Original Article
  • Published:
Annals of Microbiology Aims and scope Submit manuscript

Abstract

The consumption of probiotic-based products has risen greatly in recent decades. Due to their probiotic characteristics, microorganisms such as lactobacilli and bifidobacteria are in daily use in the production of food supplements. In the present study, three bifidobacterial strains (Bifidobacterium breve M-16 V, Bifidobacterium longum subsp. infantis M-63 and Bifidobacterium longum subsp. longum BB536) were tested for growth compatibility, resistance to antimicrobial agents, antibacterial activity against pathogens, resistance to gastric acidity, bile salt hydrolysis and adhesion to the human intestinal epithelial cell line HT29. All of these strains were resistant to gentamycin, but none showed in vitro growth incompatibility or the presence of known resistance determinants. B. breve M-16 V had the best probiotic characteristics and, indeed, was the only strain possessing antibacterial activity against Escherichia coli and Klebsiella pneumoniae. All strains were resistant to simulated gastric juice, while only B. longum subsp. longum BB536 and B. breve M-16 V showed a bile salt hydrolytic activity. Interestingly, a strong adhesion to HT29 cells was observed in all Bifidobacterium strains. In conclusion, B. breve M-16 V, B. longum subsp. longum BB536 and B. longum subsp. infantis M-63 showed several promising characteristics as probiotic strains.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1a,b
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Begley M, Hill C, Gahan CG (2006) Bile salt hydrolase activity in probiotics. Appl Environ Microbiol 72:1729–1738

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bernet MF, Brassart D, Neeser JR, Servin AL (1993) Adhesion of human bifidobacterial strains to cultured human intestinal epithelial cells and inhibition of enteropathogen-cell interactions. Appl Environ Microbiol 59:4121–4128

    PubMed Central  CAS  PubMed  Google Scholar 

  • Campos J, Mourão J, Pestana N, Peixe L, Novais C, Anyunes P (2013) Microbiological quality of ready-to-eat salads: an underestimated vehicle of bacteria and clinically relevant antibiotic resistance genes. Int J Food Microbiol 166:464–470

    Article  PubMed  Google Scholar 

  • Caplice E, Fitzgerald GF (1999) Food fermentations: role of microorganisms in food production and preservation. Int J Food Microbiol 50:131–149

    Article  CAS  PubMed  Google Scholar 

  • Charteris WP, Kelly PM, Morelli L, Collins JK (1998) Development and application of an in vitro methodology to determine the transit tolerance of potentially probiotic Lactobacillus and Bifidobacterium species in the upper human gastrointestinal tract. J Appl Microbiol 84:759–768

    Article  CAS  PubMed  Google Scholar 

  • Collado MC, Sanz Y (2007) Induction of acid resistance in Bifidobacterium: a mechanism for improving desirable traits of potentially probiotic strains. J Appl Microbiol 103:1147–1157

    Article  CAS  PubMed  Google Scholar 

  • Collado MC, Gueimonde M, Hernández M, Sanz Y, Salminen S (2005) Adhesion of selected Bifidobacterium strains to human intestinal mucus and the role of adhesion in enteropathogen exclusion. J Food Prot 68:2672–2678

    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

    Article  CAS  PubMed  Google Scholar 

  • Del Re B, Sgorbati B, Miglioli M, Palenzona D (2000) Adhesion, autoaggregation and hydrophobicity of 13 strains of Bifidobacterium longum. Lett Appl Microbiol 31:438–442

    Article  PubMed  Google Scholar 

  • Devirgiliis C, Barile S, Perozzi G (2011) Antibiotic resistance determinants in the interplay between food and gut microbiota. Genes Nutr 6:275–284

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Drago L, Mattina R, De Vecchi E, Toscano M (2013) Phenotypic and genotypic antibiotic resistance in some probiotics proposed for medical use. Int J Antimicrob Agents 41:396–367

    Article  CAS  PubMed  Google Scholar 

  • EFSA (2008) The maintenance of the list of QPS microorganisms intentionally added to food or feed. Scientific opinion of the panel on biological hazards. EFSA J 923:1–48

    Google Scholar 

  • Gibson GR, Fuller R (2000) Aspects of in vitro and in vivo research approaches directed toward identifying probiotics and prebiotics for human use. J Nutr 130:391–365

    Google Scholar 

  • Ibrahim SA, Dharmavaram SR, Seo CW, Shahbazi G (2005) Antimicrobial activity of Bifidobacterium longum (NCFB 2259) as influenced by spices. Int J Food Safety 2:6–8

    Google Scholar 

  • Ishizeki S, Sugita M, Takata M, Yaeshima T (2013) Effect of administration of bifidobacteria on intestinal microbiota in low-birth-weight infants and transition of administered bifidobacteria: a comparison between one-species and three-species administration. Anaerobe 23:38–44

    Article  PubMed  Google Scholar 

  • Jonasson J, Olofsson M, Monstein HJ (2002) Classification, identification and subtyping of bacteria based on pyrosequencing and signatura matching of 16S rDNA fragments. APMIS 110:263–272

    Article  CAS  PubMed  Google Scholar 

  • Keller MK, Bardow A, Jensdottir T, Lykkeaa J, Twetman S (2012) Effect of chewing gums containing the probiotic bacterium Lactobacillus reuteri on oral malodour. Acta Odontol Scand 70:246–250

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi N, Alam M, Nishimoto Y, Urasawa S, Uehara N, Watanabe N (2001) Distribution of aminoglycoside resistance genes in recent clinical isolates of Enterococcus faecalis, Enterococcus faecium and Enterococcus avium. Epidemiol Infect 126:197–204

    Article  PubMed Central  CAS  PubMed  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 

  • Mach T (2006) Clinical usefulness of probiotics against chronic inflammatory bowel diseases. J Physiol Pharmacol 57:23–33

    PubMed  Google Scholar 

  • Makras L, De Vuyst L (2006) The in vitro inhibition of Gram-negative pathogenic bacteria by bifidobacteria is caused by the production of organic acids. Int J Dairy Sci 16:1049–1057

    Article  CAS  Google Scholar 

  • Matsumoto M, Ohishi H, Benno Y (2004) H + −ATPase activity in Bifidobacterium with special reference to acid tolerance. Int J Food Microbiol 93:109–113

    Article  CAS  PubMed  Google Scholar 

  • Maus JE, Ingham SC (2003) Employment of stressful conditions during culture production to enhance subsequent cold- and acid-tolerance of bifidobacteria. J Appl Microbiol 95:146–154

    Article  CAS  PubMed  Google Scholar 

  • Mayo B, van Sinderen D (2010) Bifidobacteria: genomics and molecular aspects. Caister Academic, Norwich, UK

  • Moubareck C, Gavini F, Vaugien L, Butel MJ, Doucet-Populaire F (2005) Antimicrobial susceptibility of bifidobacteria. J Antimicrob Chemother 55:38–44

    Article  CAS  PubMed  Google Scholar 

  • National Committee for Clinical Laboratory Standards (2003) Performance standards for antimicrobial susceptibility testing; 13th informational supplement M 100-S 13. NCCLS, Villanova

    Google Scholar 

  • Ouoba L, Lei V, Jensen L (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 121:217–24

    Article  CAS  PubMed  Google Scholar 

  • Ouwehand AC, Salminen S, Isolauri E (2002) Probiotics: an overview of beneficial effects. Antonie Van Leeuewenhoek 82:279–289

    Article  CAS  Google Scholar 

  • Reid G (2008) Probiotic lactobacilli for urogenital health in women. J Clin Gastroenterol 42:234–236

    Article  Google Scholar 

  • Rowland I, Capurso L, Collins K, Cummings J, Delzenne N, Goulet O, Guarner F, Marteau P, Meier R (2009) Current level of consensus on probiotic science-report of an expert meeting-London, 23 November 2009. Gut Microbes 1:436–439

    Article  Google Scholar 

  • Satoh Y, Shinohara K, Umezaki H (2007) Bifidobacteria prevents necrotizing enterocolitis and infection in preterm infants. Int J Probiot Prebiot 2:149–154

    Google Scholar 

  • Satokari RM, Vaughan EE, Smidt H, Saarela M, Mättö J, de Vos WM (2003) Molecular approaches for the detection and identification of bifidobacteria and lactobacilli in the human gastrointestinal tract. System Appl Microbiol 26:572–584

    Article  CAS  Google Scholar 

  • Schillinger U, Guigas C, Holzapfel WH (2004) In vitro adherence and other properties of lactobacilli used in probiotic yoghurt-like products. Int Dairy J 15:1289–1297

    Article  Google Scholar 

  • Schoster A, Kokotovic B, Permin A, Pedersen PD, Dal Bello F, Guardabassi L (2013) In vitro inhibition of Clostridium difficile and Clostridium perfringens by commercial probiotic strains. Anaerobe 20:36–41

    Article  CAS  PubMed  Google Scholar 

  • Styriak I, Nemcová R, Chang YH, Ljungh A (2003) Binding of extracellular matrix molecules by probiotic bacteria. Lett Appl Microbiol 37:329–333

    Article  CAS  PubMed  Google Scholar 

  • Tanaka H, Doesburg K, Iwasaki T, Mierau I (1999) Screening of lactic acid bacteria for bile salt hydrolase activity. J Dairy Sci 82:2530–2535

    Article  CAS  PubMed  Google Scholar 

  • Tejero-Sariñena S, Barlowb J, Costabile A, Gibson GR, Rowland I (2012) In vitro evaluation of the antimicrobial activity of a range of probiotics against pathogens: evidence for the effects of organic acids. Anaerobe 18:530–538

    Article  PubMed  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  PubMed  Google Scholar 

  • Teuber M, Meile L, Schwarz F (1999) Acquired antibiotic resistance in lactic acid bacteria from food. Antonie Van Leeuwenhoek 76:115–137

    Article  CAS  PubMed  Google Scholar 

  • Toscano M, de Vecchi E, Rodighiero V, Drago L (2011) Microbiological and genetic identification of some probiotics proposed for medical use in 2011. J Chemother 25:156–161

    Article  Google Scholar 

  • Vanderhoof JA (2008) Probiotics in allergy management. J Pediatr Gastroenterol Nutr 47:38–40

    Article  Google Scholar 

  • Westerlund B, Korhonen TK (1993) Bacterial proteins binding to the mammalian extracellular matrix. Mol Microbiol 9:687–694

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lorenzo Drago.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Toscano, M., De Vecchi, E., Gabrieli, A. et al. Probiotic characteristics and in vitro compatibility of a combination of Bifidobacterium breve M-16 V, Bifidobacterium longum subsp. infantis M-63 and Bifidobacterium longum subsp. longum BB536. Ann Microbiol 65, 1079–1086 (2015). https://doi.org/10.1007/s13213-014-0953-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13213-014-0953-5

Keywords

Navigation