Skip to main content
SpringerLink
Log in

Substrate preference of Bifidobacterium adolescentis MB 239: compared growth on single and mixed carbohydrates

  • Applied Microbial and Cell Physiology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

The utilization of mono-, di-, and oligosaccharides by Bifidobacterium adolescentis MB 239 was investigated. Raffinose, fructooligosaccharides (FOS), lactose, and the monomeric moieties glucose and fructose were used. To establish a hierarchy of sugars preference, the kinetics of growth and sugar consumption were determined on individual and mixed carbohydrates. On single carbon sources, higher specific growth rates and cell yields were attained on di- and oligosaccharides compared to monosaccharides. Analysis of the carbohydrates in steady-state chemostat cultures, growing at the same dilution rate on FOS, lactose, or raffinose, showed that monomeric units and hydrolysis products were present. In chemostat cultures on individual carbohydrates, B. adolescentis MB 239 simultaneously displayed α-galactosidase, β-galactosidase, and β-fructofuranosidase activities on all the sugars, including monosaccharides. Glycosyl hydrolytic activities were found in cytosol, cell surface, and growth medium. Batch experiments on mixtures of carbohydrates showed that they were co-metabolized by B. adolescentis MB 239, even if different disappearance kinetics were registered. When mono-, di-, and oligosaccharides were simultaneously present in the medium, no precedence for monosaccharides utilization was observed, and di- and oligosaccharides were consumed before their constitutive moieties.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Bruckner R, Titgemeyer F (2002) Carbon catabolite repression in bacteria: choice of the carbon source and autoregulatory limitation of sugar utilization. FEMS Microbiol Lett 209:141–148

    Article  CAS  Google Scholar 

  • Crociani F, Alessandrini A, Mucci MM, Biavati B (1994) Degradation of complex carbohydrates by Bifidobacterium spp. Int J Food Microbiol 24:199–210

    Article  CAS  Google Scholar 

  • Degnan BA, Macfarlane GT (1991) Comparison of carbohydrate substrate preferences in eight species of bifidobacteria. FEMS Microbiol Lett 68:151–156

    Article  CAS  Google Scholar 

  • Degnan B A, Macfarlane GT (1993) Transport and metabolism of glucose and arabinose in Bifidobacterium breve. Arch Microbiol 160:144–151

    Article  CAS  Google Scholar 

  • Derensy-Dron D, Krzewinski F, Brassart C, Bouquelet S (1999)Beta-1,3-galactosyl-N-acetylhexosamine phosphorylase from Bifidobacterium bifidum DSM 20082: characterization, partial purification and relation to mucin degradation. Biotechnol Appl Biochem 29:3–10

    CAS  Google Scholar 

  • Ehrmann MA, Korakli M, Vogel RF (2003) dentification of the gene for beta-fructofuranosidase of Bifidobacterium lactis DSM10140(T) and characterization of the enzyme expressed in Escherichia coli. Curr Microbiol 46:391–397

    Article  CAS  Google Scholar 

  • Gibson GR, Wang X (1994) Bifidogenic properties of different types of fructo-oligosaccharides. Food Microbiol 11:491–498

    Article  CAS  Google Scholar 

  • Hinz SW, van den Broek LA, Beldman G, Vincken JP, Voragen AG (2004) beta-Galactosidase from Bifidobacterium adolescentis DSM20083 prefers beta(1,4)-galactosides over lactose. Appl Microbiol Biotechnol 66:276–284

    Article  CAS  Google Scholar 

  • Hopkins MJ, Cummings JH, McFarlane GT (1998) Inter-species differences in maximum specific growth rates and cell yields of bifidobacteria cultured on oligosaccharides and other simple carbohydrate sources. J Appl Microbiol 85:381–386

    Article  CAS  Google Scholar 

  • Janer C, Rohr LM, Pelaez C, Laloi M, Cleusix V, Requena T, Meile L (2004) Hydrolysis of oligofructoses by the recombinant β-fructofuranosidase from Bifidobacterium lactis. System Appl Microbiol 27:279–285

    Article  CAS  Google Scholar 

  • Jork H, Funk W, Fischer W, Wimmer H (1990) Thin layer chromatography: reagents and detection methods, vol. 1a. VCH, Weinheim, Germany

    Google Scholar 

  • Kaster AG, Brown LR (1983) Extracellular dextranase activity produced by human oral strains of the genus Bifidobacterium. Infect Immun 42:716–720

    CAS  Google Scholar 

  • Katayama T, Sakuma A, Kimura T, Makimura Y, Hiratake J, Sakata K, Yamanoi T, Kumagai H, Yamamoto K (2004) Molecular cloning and characterization of Bifidobacterium bifidum 1,2-alpha-l-fucosidase (AfcA), a novel inverting glycosidase (glycoside hydrolase family 95). J Bacteriol 186:4885–4893

    Article  CAS  Google Scholar 

  • Kim TB, Song SH, Kang SC, Oh DK (2003) Quantitative comparison of lactose and glucose utilization in Bifidobacterium longum cultures. Biotechnol Prog 19:672–675

    Article  CAS  Google Scholar 

  • Kovarova-Kovar K, Egli T (1998) Growth kinetics of suspended microbial cells: from single-substrate-controlled growth to mixed substrate kinetics. Microbiol Mol Biol Rev 1998 62:646–666

    CAS  Google Scholar 

  • Krzewinski F, Brassart C, Gavini F, Bouquelet S (1996) Characterization of the lactose transport system in the strain Bifidobacterium bifidum DSM 20082. Curr Microbiol 32:301:307

    Article  Google Scholar 

  • Krzewinski F, Brassart C, Gavini F, Bouquelet S (1997) Glucose and galactose transport in Bifidobacterium bifidum DSM 20082. Curr Microbiol 35:175–179

    Article  CAS  Google Scholar 

  • Leder S, Hartmeier W, Marx SP (1999) α-galactosidase of Bifidobacterium adolescentis DSM 20083. Curr Microbiol 38:101–106

    Article  CAS  Google Scholar 

  • Lee SK, Kim YB, Ji GE (1997) Note: purification of amylase secreted from Bifidobacterium adolescentis. J Appl Microbiol 83:267–272

    Article  CAS  Google Scholar 

  • Margolles A, de los Reyes-Galivàn CG (2003) Purification and functional characterization of a novel α-l-Arabinofuranosidase from Bifidobacterium longum B667. Appl Environ Microbiol 69:5096–5103

    Article  CAS  Google Scholar 

  • Mlobeli NT, Gutierrez NA, Maddox IS (1998) Physiology and kinetics of Bifidobacterium bifidum during growth on different sugars. Appl Microbiol Biotechnol 50:125–128

    Article  CAS  Google Scholar 

  • Moller PL, Jorgensen F, Hansen OC, Madsen SM, Stougaard P (2001) Intra- and extracellular beta-galactosidases from Bifidobacterium bifidum and B. infantis: molecular cloning, heterologous expression, and comparative characterization. Appl Environ Microbiol 67:2276–2283

    Article  CAS  Google Scholar 

  • Murphy O (2001) Non-polyol low-digestible carbohydrates: food applications and functional benefits. Br J Nutr 85:47–53

    Article  Google Scholar 

  • Narang A, Konopka A, Ramkrishna D (1997) The dynamics of microbial growth on mixtures of substrates in batch reactors. J Theor Biol 184:301–317

    Article  CAS  Google Scholar 

  • Palframan RJ, Gibson GR, Rastall RA (2003) Carbohydrate preferences of Bifidobacterium species isolated from the human gut. Curr Issues Intest Microbiol 4:71–75

    CAS  Google Scholar 

  • Perrin S, Warchol M, Grill JP, Schneider F (2001) Fermentations of fructo-oligosaccharides and their components by Bifidobacterium infantis ATCC 15697 on batch culture in semi-synthetic medium. J Appl Microbiol 90:859–865

    Article  CAS  Google Scholar 

  • Rada V, Bartonova J, Vlkova E (2002) Specific growth rate of bifidobacteria cultured on different sugars. Folia Microbiol (Praha) 47:477–480

    CAS  Google Scholar 

  • Rossi M, Altomare A, Gonzalez Vara y Rodriguez A, Brigidi P, Matteuzzi D (2000) Nucleotide sequence, expression and trascriptional analysis of the Bifidobacterium longum MB 219 lacZ gene. Arch Microbiol 174:74–80

    Article  CAS  Google Scholar 

  • Rossi M, Corradini C, Amaretti A, Nicolini M, Pompei A, Zanoni S, Matteuzzi D (2005) Fermentation of fructooligosaccharides and inulin by bifidobacteria: a comparative study in pure and faecal cultures. Appl Environ Microbiol 71:6150–6158

    Article  CAS  Google Scholar 

  • Saier MH Jr (1997) Multiple mechanisms controlling carbon metabolism in bacteria. Biotechnol Bioeng 58:170–174

    Article  Google Scholar 

  • Saier MH Jr, Chauvaux S, Cook GM, Deutscher J, Paulsen IT, Reizer J, Ye J (1996) Catabolite repression and inducer control in Gram-positive bacteria. Microbiol 142:217–230

    Article  CAS  Google Scholar 

  • Salminen S, Bouley C, Boutron-Ruault MC, Cummings JH, Franck A, Gibson GR, Isolauri E, Moreau MC, Roberfroid M, Rowland I (1998) Functional food science and gastrointestinal physiology and function. Br J Nutr 80:S147–S171

    Article  CAS  Google Scholar 

  • Scardovi V (1986) Genus Bifidobacterium. In: Sneath H, Mair N, Sharpe M, Holt J (eds) Bergey’s manual of systematic bacteriology, vol 2, 9th edn. Williams & Wilkins, Baltimore, MD, pp 1418–1434

    Google Scholar 

  • Schell MA, Karmirantzou M, Snel B, Vilanova D, Berger B, Pessi G, Zwahlen MC, Desiere F, Bork P, Delley M, Pridmore RD, Arigoni F (2002) The genome sequence of Bifidobacterium longum reflects its adaptation to the human gastrointestinal tract. Proc Natl Acad Sci U S A 99:14422–14427

    Article  CAS  Google Scholar 

  • Shene C, Mardones M, Zamora P, Bravo S (2005) Kinetics of Bifidobacterium longum ATCC 15707 fermentations: effect of the dilution rate and carbon source. Appl Microbiol Biotechnol 67:623–630

    Article  CAS  Google Scholar 

  • Slovakova L, Duskova D, Marounek M (2002) Fermentation of pectin and glucose, and activity of pectin-degrading enzymes in the rabbit caecal bacterium Bifidobacterium pseudolongum. Lett Appl Microbiol 35:126–130

    Article  CAS  Google Scholar 

  • Tannock GV (1999) Probiotics. A critical review. Horizon Scientific, Norfolk, UK

    Google Scholar 

  • Tannock GV (2002) Probiotics and prebiotics. Where are we going? Caister Academic, Norfolk, UK

    Google Scholar 

  • van den Broek L, Struijs K, Verdoes J, Beldman G, Voragen A (2003) Cloning and characterization of two α-glucosidases from Bifidobacterium adolescentis DSM20083. Appl Microbiol Biotechnol 61:55–60

    Google Scholar 

  • van den Broek LAM, Lloyd RM, Beldman G, Verdoes JC, McCleary BV, Voragen AGJ (2005) Cloning and characterization of arabinoxylan arabinofuranohydrolase-D3 (AXHd3) from Bifidobacterium adolescentis DSM20083 Appl Microbiol Biotechnol 67:641–647

    Article  CAS  Google Scholar 

  • van der Meulen R, Avonts L, de Vuyst L (2004) Short fractions of oligofructose are preferentially metabolized by Bifidobacterium animalis DN-173 010. Appl Environ Microbiol 70:1923–1930

    Article  CAS  Google Scholar 

  • van Laere KMJ, Hartemink R, Beldman G, Pitson S, Dijema C, Schols HA, Voragen AGJ (1999) Transglycosidase activity of Bifidobacterium adolescentis DSM 20083 α-galactosidase. Appl Microbiol Biotechnol 52:681–688

    Article  Google Scholar 

  • Wang X, Conway PL, Brown IL, Evans AJ (1999) In vitro utilization of amylopectin and high-amylose maize (Amylomaize) starch granules by human colonic bacteria. Appl Environ Microbiol 65:4848–4854

    CAS  Google Scholar 

  • Warchol M, Perrin S, Grill JP, Schneider F (2002) Characterization of a purified β-fructofuranosidase from Bifidobacterium infantis ATCC 15697. Lett Appl Microbiol 35:462–467

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Pharmaceutical Sciences, University of Bologna, Bologna, Italy

    Alberto Amaretti, Anna Pompei, Simona Zanoni & Diego Matteuzzi

  2. Department of Chemistry, University of Ferrara, Ferrara, Italy

    Elena Tamburini, Tatiana Bernardi & Giuseppe Vaccari

  3. Department of Chemistry, University of Modena and Reggio Emilia, Via Campi 183, 41100, Modena, Italy

    Maddalena Rossi

Authors
  1. Alberto Amaretti
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Elena Tamburini
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tatiana Bernardi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Anna Pompei
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Simona Zanoni
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Giuseppe Vaccari
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Diego Matteuzzi
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Maddalena Rossi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maddalena Rossi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Amaretti, A., Tamburini, E., Bernardi, T. et al. Substrate preference of Bifidobacterium adolescentis MB 239: compared growth on single and mixed carbohydrates. Appl Microbiol Biotechnol 73, 654–662 (2006). https://doi.org/10.1007/s00253-006-0500-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-006-0500-9

Keywords

Search

Navigation