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Induction of α-l-arabinofuranosidase activity by monomeric carbohydrates in Bifidobacterium longum and ubiquity of encoding genes

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Abstract

Bifidobacterium longum can be isolated from human faeces, some strains being considered probiotics. B. longum NIZO B667 produces an exo-acting α-l-arabinofuranosidase, AbfB, previously purified by us, that releases l-arabinose from arabinan and arabinoxylan. This activity was subjected to two–seven-fold induction by l-arabinose, d-xylose, l-arabitol and xylitol and to repression by glucose. Maximum activity was obtained at 48 h incubation except for d-xylose that was at 24 h. High concentrations (200 mM) of l-arabitol also caused repression of the arabinofuranosidase. A unique band of activity showing the same migration pattern as the purified AbfB was found in zymograms of cell free extracts, indicating that the activity was likely due to this sole enzyme. The assessment of the influence of inducers and repressors on the activity of AbfB and on the expression of the abfB gene by real time PCR indicated that regulation was transcriptional. DNA amplifications using a pair of degenerated primers flanking an internal fragment within α-l-arabinofuranosidase genes of the family 51 of glycoside hydrolases evidenced that these enzymes are widespread in Bifidobacterium. The aminoacidic sequences of bifidobacteria included a fragment of four to six residues in the position 136–141 that was absent in other microorganisms

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References

  • Ali S, Sayed A (1992) Regulation of cellulase biosynthesis in Aspergillus terreus. World J Microbiol Biotechnol 8:73–75

    Article  CAS  Google Scholar 

  • Belenguer A, Duncan SH, Graham Calder A, Holtrop G, Louis P, Lobley GE, Flint HJ (2006) Two routes of metabolic cross-feeding between Bifidobacterium adolescentis and butyrate-producing anaerobes from the human gut. Appl Environ Microbiol 72: 3593–3599

    Article  PubMed  CAS  Google Scholar 

  • Carvallo M, de Ioannes P, Navarro C, Chavez R, Peirano A, Bull P, Eyzaguirre J (2003) Characterization of an alpha-l-arabinofuranosidase gene (abf1) from Penicillium purpurogenum and its expression. Mycol Res 107:388–394

    Article  PubMed  CAS  Google Scholar 

  • Clinche FL, Piñaga F, Ramón D, Vallés S (1997) α-l-arabinofuranosidases from Aspergillus terreus with potential application in enology: induction, purification, and characterization. J Agric Food Chem 45:2379–2383

    Article  Google Scholar 

  • Cummings JH, Englyst H (1995) Gastrointestinal effects of food carbohydrates. Am J Clin Nutr 61:938S–945S

    PubMed  CAS  Google Scholar 

  • De Ioannes P, Peirano A, Steiner J, Eyzaguirre J (2000) An α-l-arabinofuranosidase from Penicillium purpurogenum: production, purification and properties. J Biotechnol 76:253–258

    Article  PubMed  Google Scholar 

  • De Vries RP, van den Broeck HC, Dekkers E, Manzanares P, de Graff LH, Visser J. (1999) Differential expression of three alpha-galactosidase genes and a single beta-galactosidase gene from Aspergillus niger. Appl Environ Microbiol 65:2453–2460

    PubMed  Google Scholar 

  • FilhoEX, Puls J, Coughlan MP (1996) Purification and characterization of two arabinofuranosidases from solid-state cultures of the fungus Penicillium capsulatum. Appl Environ Microbiol 62:168–173

    Google Scholar 

  • Gibson GR, Roberfroid MB (1995) Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr 125:1401–1412

    PubMed  CAS  Google Scholar 

  • Gielkens M, González-Candelas L, Sánchez-Torres P, van de Vondervoort P, de Graaff L, Visser J, Ramón D (1999) The abfB gene encoding the major α-l-arabinofuranosidase of Aspergillus nidulans: nucleotide sequence, regulation and construction of a disrupted strain. Microbiology 145:735–741

    PubMed  CAS  Google Scholar 

  • Gueimonde M, Tölkkö S, Korpimäki T, Salminen S (2004) New real-time quantitative PCR procedure for quantification of bifidobacteria in human fecal samples. Appl Environ Microbiol 70:4165–4169

    Article  PubMed  CAS  Google Scholar 

  • Gueimonde M, Debor L, Tölkkö S, Jokisalo E, Salminen S (2006) Quantitative assessment of faecal bifidobacterial populations by real-time PCR using lanthanide probes. J Appl Microbiol (In press)

  • Higashi K, Kusakabe I, Yasui T, Ishiyama T, Okimoto Y (1983) Arabinan-degrading enzymes from Streptomyces diastatochromogenes 065. Agric Biol Chem 47:2903–2905

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Luonteri E, Siika-aho M, Tenkanen M, Viikari L (1995) Purification and characterization of three α-l-arabinofuranosidases from Aspergillus terreus. J Biotechnol 38:279–291

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Mota LJ, Tavares P, Sá-Nogueira I (1999) Mode of action of AraR, the key regulator of L-arabinose metabolism in Bacillus subtilis. Mol Microbiol 33:476–489

    Article  PubMed  CAS  Google Scholar 

  • Orejas M, MacCabe AP, Pérez González JA, Kumar S, Ramón D (1999) Carbon catabolite repression of the Aspergillus nidulans xlnA gene. Mol Microbiol 31:177–184

    Article  PubMed  CAS  Google Scholar 

  • Pitson SM, Voragen AG, Beldman G (1996) Stereochemical course of hydrolysis catalyzed by arabinofuranosyl hydrolases. FEBS Lett 398:7–11

    Article  PubMed  CAS  Google Scholar 

  • Ramón D, van der Veen P, Visser J (1993) Arabinan degrading enzymes from Aspergillus nidulans: induction and purification. FEMS Microbiol Lett 113:15–22

    Article  PubMed  Google Scholar 

  • Raposo MP, Inacio JM, Mota LJ, Sá-Nogueira I (2004) Transcriptional regulation of genes encoding arabinan-degrading enzymes in Bacillus subtilis. J Bacteriol 186:1287–1296

    Article  PubMed  CAS  Google Scholar 

  • Rombouts FM, Voragen AGJ, Searle-van Leeuwen MJF, Geraeds CCJM, Schols HA, Pilnik W (1988) The arabinases of Aspergillus niger: purification and characterization of two α-l-arabinofuranosidases and an endo-1, 5-α-l-arabinase. Carbohydr Polym 9:25–47

    Article  CAS  Google Scholar 

  • Saha BC, Bothast RJ (1998) Purification and characterization of a novel thermostable α-l-arabinofuranosidase from a color-variant strain of Aureobasidium pullulans. Appl Environ Microbiol 64:216–220

    PubMed  CAS  Google Scholar 

  • Saha BC (2000) α-l-Arabinofuranosidases: biochemistry, molecular biology and application in biotechnology. Biotechnol Adv 18:403–423

    Article  PubMed  CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. 2nd edn. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • SaNogueira I, Nogueira TV, Soares S, deLencastre H (1997) The Bacillus subtilis l-arabinose (ara) operon: nucleotide sequence, genetic organization and expression. Microbiology 143:957–969

    Article  CAS  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 USA. 99:14422–14427

    Article  PubMed  CAS  Google Scholar 

  • Shin HY, Park SY, Sung JH, Kim DH (2003) Purification and characterization of α-l-arabinopyranosidase and α-l-arabinofuranosidase from Bifidobacterium breve K-110, a human intestinal anaerobic bacterium metabolizing ginsenoside Rb2 and Rc. Appl Environ Microbiol 69:7116–7123

    Article  PubMed  CAS  Google Scholar 

  • Tannock GW (1995) Microecology of the gastrointestinal tract in relation to lactic acid bacteria. Int Dairy J 5:1059–1070

    Article  Google Scholar 

  • Van den Broek LAM, Lloyd RM, Geldman 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  PubMed  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  PubMed  CAS  Google Scholar 

  • Van der Veen P, Flipphi MJA, Voragen AGJ, Visser J (1991) Induction, purification and characterization of arabinases produced by Aspergillus niger. Arch Microbiol 157:23–28

    Article  Google Scholar 

  • Van der Veen P, Flipphi MJ, Voragen AG, Visser J (1993) Induction of extracellular arabinases on monomeric substrates in Aspergillus niger. Arch Microbiol 159:66–71

    Article  PubMed  Google Scholar 

  • Van der Veen P, Arst Jr HN, Flipphi MJA, Visser J (1994) Extracellular arabinases in Aspergillus nidulans: the effect of different cre mutations on enzyme levels. Arch Microbiol 162:433–440

    PubMed  Google Scholar 

  • Van Laere KM, Beldman G, Voragen AG (1997) A new arabinofuranohydrolase from Bifidobacterium adolescentis able to remove arabinosyl residues from double-substituted xylose units in arabinoxylan. Appl Microbiol Biotechnol 47:231–235

    Article  PubMed  Google Scholar 

  • Van Laere KM, Voragen CHL, Kroef T, van den Broek LAM, Beldman G, Voragen AG (1999) Purification and mode of action of two different arabinoxylan arabinofuranohydrolases from Bifidobacterium adolescentis DSM 20083. Appl Microbiol Biotechnol 51:606–613

    Article  Google Scholar 

  • Van Laere KM, Hartemink R, Bosveld M, Schols HA, Voragen AG (2000) Fermentation of plant cell wall derived polysaccharides and their corresponding oligosaccharides by intestinal bacteria. J Agric Food Chem 48:1644–1652

    Article  PubMed  CAS  Google Scholar 

  • Witteveen CFB, Busink R, van de Vondervoort P, Dijkema C, Swart K, Visser J (1989) l-arabinose and d-xylose catabolism in Aspergillus niger. J Gen Microbiol 135:2163–2171

    CAS  Google Scholar 

Download references

Acknowledgments

This work was financed by European Union FEDER funds and the Spanish Plan Nacional de I + D (project AGL2004-06088-C02-01/ALI). L. Noriega was the recipient of a predoctoral fellowship from Fundación para la Investigación Científica y Técnica (FICYT, Asturias, Spain). M. Gueimonde was funded by a Juan de la Cierva postdoctoral contract from the Spanish Ministry of Education and Science.

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Correspondence to Clara G. de los Reyes-Gavilán.

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Gueimonde, M., Noriega, L., Margolles, A. et al. Induction of α-l-arabinofuranosidase activity by monomeric carbohydrates in Bifidobacterium longum and ubiquity of encoding genes. Arch Microbiol 187, 145–153 (2007). https://doi.org/10.1007/s00203-006-0181-x

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  • DOI: https://doi.org/10.1007/s00203-006-0181-x

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