Skip to main content
Log in

Conditions affecting cell surface properties of human intestinal bifidobacteria

  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

The cell surface properties of human intestinal bifidobacteria have been characterized for 30 strains isolated from a fecal sample. Strain identification to the species level was obtained by restriction analysis of the amplified 16S rRNA gene and confirmed by DNA/DNA reassociation experiments. The isolates were grouped in four genetically homogeneous clusters whose members belonged to Bifidobacterium bifidum, Bifidobacterium adolescentis, Bifidobacterium longum and Bifidobacterium pseudocatenulatum species. Cell surface properties of Bifidobacterium strains were evaluated by determining the level of hydrophobicity, adhesion to hydrocarbons and contact angle measurements, and their autoaggregation ability. The results showed high and homogeneous level of hydrophobicity in all tested strains when contact angle measurements values were considered. On the contrary, autoaggregation assays and bacterial adhesion to hydrocarbons detected interesting differences in cell surface properties among the tested Bifidobacterium strains. The highest levels of autoaggregation, detected in B. bifidum and B. adolescentis strains, were strictly dependent on the pH of the medium. Moreover, protease treatment experiments suggested that proteins had a key role in the autoaggregating ability of B. bifidum and B. adolescentis 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.

Similar content being viewed by others

References

  • M. Alander R. Satokari R. Korpela M. Saxelin T. Vilpponen-Salmela T. Mattila-Sandholm A. Wright Particlevon (1999) ArticleTitlePersistence of colonization of human colonic mucosa by a probiotic strain, Lactobacillus rhamnosus GG, after oral consumption Appl. Environ. Microbiol. 65 351–354 Occurrence Handle9872808 Occurrence Handle1:CAS:528:DyaK1MXjvVylsA%3D%3D

    PubMed  CAS  Google Scholar 

  • H. Beerens (1990) ArticleTitleAn elective and selective isolation medium for Bifidobacterium Spp Lett. Appl. Microbiol. 11 155–157

    Google Scholar 

  • M.-F. Bernet D. Brassart J.-R. Neeser A.L. Servin (1993) ArticleTitleAdhesion of human bifidobacterial strains to cultured human intestinal epithelial cells and inhibition of enteropathogen-cell interactions Appl. Environ. Microbiol. 59 4121–4128 Occurrence Handle8285709 Occurrence Handle1:CAS:528:DyaK2cXltFWgtQ%3D%3D

    PubMed  CAS  Google Scholar 

  • H.J. Busscher B. Belt-Gritter Particlevan de H.C. Mei Particlevan der (1995) ArticleTitleImplications of microbial adhesion to hydrocarbons for evaluating cell surface hydrophobicity. 1. Zeta potentials of hydrocarbon droplets Colloids surf. B. Biointerfaces 5 111–116 Occurrence Handle1:CAS:528:DyaK2MXpsV2mur0%3D

    CAS  Google Scholar 

  • D. Daffonchio J. Thaveesri W. Verstraete (1995) ArticleTitleContact Angle Measureme nt and cell hydrophobicity of granular sludge from upflow anaerobic sludge bed reactors Appl. Environ. Microbiol. 61 3676–3680 Occurrence Handle1:CAS:528:DyaK2MXosFGms7w%3D Occurrence Handle16535148

    CAS  PubMed  Google Scholar 

  • B. Re ParticleDel A. Busetto G. Vignola B. Sgorbati D. Palenzona (1998) ArticleTitleAutoaggregation and adhesion ability in a Bifidobacterium suis strain Lett. Appl. Microbiol. 27 307–310 Occurrence Handle9830151

    PubMed  Google Scholar 

  • B. Re ParticleDel B. Sgorbati M. Miglioli D. Palenzona (2000) ArticleTitleAdhesion, autoaggregation and hydrophobicity of 13 strains of Bifidobacterium longum Lett. Appl. Microbiol. 31 438–442 Occurrence Handle11123552

    PubMed  Google Scholar 

  • L. Edmunds (2001) ArticleTitleThe underuse of probiotics by family physicians Can. Med. Assoc. J. 164 1577 Occurrence Handle1:STN:280:DC%2BD3MzjsFeqsQ%3D%3D

    CAS  Google Scholar 

  • G. Elmer C. Surawicz L. Macfarland (1996) ArticleTitleBiotherapeutic agents: a neglected modality for the treatment and prevention of selected intestinal and vaginal infections J. Am. Med. Assoc. 275 870–876 Occurrence Handle10.1001/jama.275.11.870 Occurrence Handle1:STN:280:BymC2szotlU%3D

    Article  CAS  Google Scholar 

  • J. Fogh J.M. Fogh T. Orfeo (1977) ArticleTitleOne hundred and twenty seven cultured tumor cell lines producing tumors in nude mice J. Natl. Cancer Inst. 59 221–226 Occurrence Handle327080 Occurrence Handle1:STN:280:CSiB3M%2FgtlA%3D

    PubMed  CAS  Google Scholar 

  • M. Freter (1992) Factors affecting the microecology of the gut R. Fuller (Eds) Probiotics. The Scientific Basis Chapman and Hall Glasgow 111–145

    Google Scholar 

  • S. Fujiwara H. Hashiba T. Hirota J.F. Forstner (1999) ArticleTitlePurification and characterization of a novel protein produced by Bifidobacterium longum SBT2928 that inhibits the binding of enterotoxigenic Escherichia coli Pb176 (CFA/II) to gangliotetraosylceramide J. Appl. Microbiol. 86 615–621 Occurrence Handle10.1046/j.1365-2672.1999.00705.x Occurrence Handle10212407 Occurrence Handle1:CAS:528:DyaK1MXivVCmsbc%3D

    Article  PubMed  CAS  Google Scholar 

  • G.I. Geertsema-Doornbusch H.C. Mei Particlevan der H.J. Busscher (1993) ArticleTitleMicrobial cell surface hydrophobicity. The involvement of electrostatic interactions in microbial adhesion to hydrocarbon (MATH) J. Microbiol. Meth. 18 61–68 Occurrence Handle10.1016/0167-7012(93)90072-P

    Article  Google Scholar 

  • G.R. Gibson X. Wang (1994) ArticleTitleRegulatory effects of bifidobacteria on the growth of other colonic bacteria J. Appl. Bacteriol. 77 412–420 Occurrence Handle7989269 Occurrence Handle1:STN:280:ByqD1c7gtlE%3D

    PubMed  CAS  Google Scholar 

  • H.S. Gill (2003) ArticleTitleProbiotics to enhance anti-infective defences in the gastrointestinal tract. Best practice and research Clin. Gastroenterol. 17 755–773 Occurrence Handle1:CAS:528:DC%2BD3sXnsVWkt7s%3D

    CAS  Google Scholar 

  • A. Gomez Zavaglia G. Kociubinski P. Perez E. Disalvo G. De Antoni (2002) ArticleTitleEffect of bile on the lipid composition and surface properties of bifidobacteria J. Appl. Microbiol. 93 794–799 Occurrence Handle10.1046/j.1365-2672.2002.01747.x Occurrence Handle12392525 Occurrence Handle1:CAS:528:DC%2BD38XptVOnurw%3D

    Article  PubMed  CAS  Google Scholar 

  • J.M. Hamilton-Miller (2003) ArticleTitleThe role of probiotics in the treatment and prevention of Helicobacter pylori infection Int. J. Antimicrob. Agents 22 360–366 Occurrence Handle14522098 Occurrence Handle1:CAS:528:DC%2BD3sXns12msL0%3D

    PubMed  CAS  Google Scholar 

  • Y. Kado-Oka S. Fujiwara T. Hirota (1991) ArticleTitleEffects of bifidobacteria cells on mitogenic response of splenocytes and several functions of phagocytes Milchwissenschaft 46 626–630

    Google Scholar 

  • B. Kos J. Suskovic S. Vukovic M. Simpraga J. Frece S. Matosic (2003) ArticleTitleAdhesion and aggregation ability of probiotic strain Lactobacillus acidophilus M92 J. Appl. Microbiol. 94 981–981 Occurrence Handle10.1046/j.1365-2672.2003.01915.x Occurrence Handle12752805 Occurrence Handle1:STN:280:DC%2BD3s3jtFajtA%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • C.P. Kurtzman C.J. Johnson M.J. Smiley (1979) ArticleTitleDetermination of conspecifcity of Candida utilis Hansenula jadinii through DNA reassociation Mycologia 71 844–847

    Google Scholar 

  • U.K. Laemmli (1970) ArticleTitleCleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 227 680–685 Occurrence Handle10.1038/227680a0 Occurrence Handle5432063 Occurrence Handle1:CAS:528:DC%2BD3MXlsFags7s%3D

    Article  PubMed  CAS  Google Scholar 

  • P.L. Manachini M.G. Fortina L. Levati C. Parini (1998) ArticleTitleContribution to phenotypic and genotypic characterization of Bacillus licheniformisdescription of new genomovars Syst. Appl. Microbiol. 21 520–529 Occurrence Handle9924820 Occurrence Handle1:CAS:528:DyaK1MXhtV2mur0%3D

    PubMed  CAS  Google Scholar 

  • P.L. Manachini S.H. Flint L.J. Ward W. Kelly M.G. Fortina C. Parini D. Mora (2002) ArticleTitleComparison between Streptococcus macedonicus Streptococcus waius strains and reclassification of Streptococcus waius (Flint et al. 1999) as Streptococcus macedonicus (Tsakalidou et al. 1998) Int. J. Syst. Evol. Microbiol. 52 945–951 Occurrence Handle12054262 Occurrence Handle1:CAS:528:DC%2BD38XkslCrurY%3D Occurrence Handle10.1099/ijs.0.02099-0

    Article  PubMed  CAS  Google Scholar 

  • M.L. Marin Y. Benito C. Pin M.F. Fernandez M.L. Garcia M.D. Selgas C. Casas (1997) ArticleTitleLactic acid bacteria: hydrophobicity and strength of attachment to meat surfaces Lett. Appl. Microbiol. 24 14–18 Occurrence Handle10.1046/j.1472-765X.1997.00334.x Occurrence Handle9023999 Occurrence Handle1:STN:280:ByiC2snksFc%3D

    Article  PubMed  CAS  Google Scholar 

  • P. Mattarelli B. Biavati F. Crociani V. Scardovi G. Prati (1993) ArticleTitleBifidobacterial cell wall proteins (BIFOP) in Bifidobacterium globosum Res. Microbiol. 144 581–590 Occurrence Handle10.1016/0923-2508(93)90008-P Occurrence Handle8310184 Occurrence Handle1:CAS:528:DyaK2cXjtFyqsbo%3D

    Article  PubMed  CAS  Google Scholar 

  • P. Mattarelli B. Biavati M. Pesenti F. Crociani (1999) ArticleTitleEffect of growth temperature on the biosynthesis of cell wall proteins from Bifidobacterium globosum Res. Microbiol. 150 117–127 Occurrence Handle10.1016/S0923-2508(99)80029-1 Occurrence Handle10209767 Occurrence Handle1:CAS:528:DyaK1MXitlent7o%3D

    Article  PubMed  CAS  Google Scholar 

  • K.B. Medrzycka (1991) ArticleTitleThe effect of particle concentration in extremely dilute solutions Prog. Colloid Polym. Sci. 269 85–90 Occurrence Handle1:CAS:528:DyaK3MXht12rsbs%3D

    CAS  Google Scholar 

  • M.A. Miller (2001) ArticleTitleProbiotics as medical therapies Can. Med. Assoc. J. 165 1470 Occurrence Handle1:STN:280:DC%2BD38%2Fjs1eisQ%3D%3D

    CAS  Google Scholar 

  • H. Noda N. Akasaka M. Ohsugi (1994) ArticleTitleBiotin production by bifidobacteria J. Nutr. Sci. Vitaminol. 40 181–188 Occurrence Handle7931726 Occurrence Handle1:CAS:528:DyaK2cXlslCrtr0%3D

    PubMed  CAS  Google Scholar 

  • H.J. Op den Camp A. Oosterhof J.H. Veerkamp (1985) ArticleTitleCell surface hydrophobicity of Bifidobacterium bifidum subsp. pennsylvanicum Antonie Van Leeuwenhoek 51 303–312 Occurrence Handle4091536 Occurrence Handle1:CAS:528:DyaL28XhtVGkur8%3D

    PubMed  CAS  Google Scholar 

  • K. Pedersen G.W. Tannock (1989) ArticleTitleColonization of the porcine gastrointestinal tract by lactobacilli Appl. Environ. Microbiol. 55 279–283 Occurrence Handle2719474 Occurrence Handle1:STN:280:BiaB2crotlw%3D

    PubMed  CAS  Google Scholar 

  • P.F. Pérez Y. Minnaard E.A. Disalvo G.L. De Antoni (1998) ArticleTitleSurface properties of bifidobacterial strains of human origin Appl. Environ. Microbiol. 64 21–26 Occurrence Handle9435057

    PubMed  Google Scholar 

  • J. Petr V. Rada (2000) ArticleTitleThe presence of autoaggregation and adhesion properties in chicken bifidobacteria strains Scientia Agriculturae Bohemica 31 233–239

    Google Scholar 

  • M. Rojas P.L. Conway (1996) ArticleTitleColonization by lactobacilli of piglet small intestinal mucus J. Appl. Bacteriol. 81 474–480 Occurrence Handle8939025 Occurrence Handle1:STN:280:ByiD1Mzks1c%3D

    PubMed  CAS  Google Scholar 

  • M. Rosenberg D. Gutnick E. Rosenberg (1980) ArticleTitleAdherence of bacteria to hydrocarbons: a simple method for measuring cell-surface hydrophobicity FEMS Microbiol. Lett. 9 29–33 Occurrence Handle10.1016/0378-1097(80)90106-8 Occurrence Handle1:CAS:528:DyaL3MXht1eqsg%3D%3D

    Article  CAS  Google Scholar 

  • V. Scardovi (1986) Genus Bifidobacterium P.H.A. Sneath N.S. Mair M.E. Sharpe J.G. Holt (Eds) Bergey's Manual of Systematic Bacteriology NumberInSeriesVol. 2 Williams and Wilkins New York 1418–1434

    Google Scholar 

  • R.J. Seidler M. Mandel (1971) ArticleTitleQuantitative aspects of deoxyribonucleic acid renaturation: base composition, state of chromosome replication and polynucleotide homologies J. bacteriol. 106 608–614 Occurrence Handle4929869 Occurrence Handle1:CAS:528:DyaE3MXhtlGitbw%3D

    PubMed  CAS  Google Scholar 

  • B. Sgorbati B. Biavati D. Palenzona (1995) The genus Bifidobacterium B.J.B. Wood W.H. Holzapfel (Eds) The Lactic Acid Bacteria NumberInSeriesVol. 2 Blackie Academic and Professional (Chapman and Hall) Glasgow 279–306

    Google Scholar 

  • K. Tahri J. Crociani J. Ballongue F. Schneider (1995) ArticleTitleEffects of three strains of bifidobacteria on cholesterol Lett. Appl. Microbiol. 21 149–151 Occurrence Handle7576497 Occurrence Handle1:CAS:528:DyaK2MXptV2ru7w%3D

    PubMed  CAS  Google Scholar 

  • R. Temmerman I. Scheirlinck G. Huys J. Swings (2003) ArticleTitleCulture-independent analysis of probiotic products by denaturing gradient gel electrophoresis Appl. Environ. Microbiol. 69 220–226 Occurrence Handle12513998 Occurrence Handle1:CAS:528:DC%2BD3sXkvVanug%3D%3D

    PubMed  CAS  Google Scholar 

  • V. Vadillo-Rodrìguez H.J. Busscher W. Norde J. Vries Particlede H.C. Mei Particlevan der (2004) ArticleTitleDynamic cell surface hydrophobicity of Lactobacillus strains with and without surface layer proteins J. Bacteriol. 186 6647–6650 Occurrence Handle15375147

    PubMed  Google Scholar 

  • van der Mei H.C., Rosenberg M. and Busscher H.J. 1991. Microbial cell surface analysis: structural and physicochemical methods. In: Mozes N., Handley P.S., Busscher H.J. and Rouxhet P.G.VCH Publishers. New York, pp. 263287.

  • H.C. Mei Particlevan der J. Vries Particlede H.J. Busscher (1993) ArticleTitleHydrophobic and electrostatic cell surface properties of thermophilic dairy streptococci Appl. Environ. Microbiol. 59 4305–4312 Occurrence Handle16349127

    PubMed  Google Scholar 

  • H.C. Mei Particlevan der B. Belt-Gritter Particlevan de H.J. Busscher (1995) ArticleTitleImplications of microbial adhesion to hydrocarbons for evaluating cell surface hydrophobicity: 2. Adhesion mechanisms Colloids surf. B. Biointerfaces 5 117–126

    Google Scholar 

  • M. Ventura M. Elli R. Reniero R. Zink (2001) ArticleTitleMolecular microbial analysis of Bifidobacterium isolates from different environments by the species-specific amplified ribosomal DNA restriction analysis (ARDRA) FEMS Microbiol. Ecol. 36 113–121 Occurrence Handle11451515 Occurrence Handle1:CAS:528:DC%2BD3MXltVeju7Y%3D

    PubMed  CAS  Google Scholar 

  • C.G. Vinderola M. Medici G. Perdigón (2004) ArticleTitleRelationship between interaction sites in the guthydrophobicity, mucosal immunomodulating capacities and cell wall protein profiles in indigenous and exogenous bacteria J. Appl. Microbiol. 96 230–243 Occurrence Handle10.1046/j.1365-2672.2004.02158.x Occurrence Handle14723684 Occurrence Handle1:CAS:528:DC%2BD2cXitVKgsb0%3D

    Article  PubMed  CAS  Google Scholar 

  • T. Wadstrom K. Andersson M. Sydow L. Axelsson S. Lindgren B. Gullmar (1987) ArticleTitleSurface properties of lactobacilli isolated from the small intestine of pigs J. Appl. Bacteriol. 62 513–520 Occurrence Handle3305459 Occurrence Handle1:STN:280:BiiA3cjnsFY%3D

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Carlo Parini.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Canzi, E., Guglielmetti, S., Mora, D. et al. Conditions affecting cell surface properties of human intestinal bifidobacteria. Antonie Van Leeuwenhoek 88, 207–219 (2005). https://doi.org/10.1007/s10482-005-6501-3

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-005-6501-3

Keywords

Navigation