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Volume 163, Issue 10

Identification of genes involved in galactooligosaccharide utilization in strain YIT 4014 Open Access

Abstract

Galactooligosaccharides (GOS) are mixed oligosaccharides that are mainly composed of galactosyllactoses (GLs), which include 3′-GL, 4′-GL, and 6′-GL. Data from numerous and studies have shown that GOS selectively stimulate the growth of bifidobacteria. Previously, we identified the gene locus responsible for 4′-GL utilization, but the selective routes of uptake and catabolism of 3′- and 6′-GL remain to be elucidated. In this study, we used differential transcriptomics to identify the utilization pathways of these GLs within the YIT 4014 strain. We found that the BBBR_RS 2305–2320 gene locus, which includes a solute-binding protein (SBP) of an ATP-binding cassette (ABC) transporter and β-galactosidase, were up-regulated during 3′- and 6′-GL utilization. The substrate specificities of these proteins were further investigated, revealing that β-galactosidase hydrolyzed both 3′-GL and 6′-GL efficiently. Our surface plasmon resonance results indicated that the SBP bound strongly to 6′-GL, but bound less tightly to 3′-GL. Therefore, we looked for the other SBPs for 3′-GL and found that the BBBR_RS08090 SBP may participate in 3′-GL transportation. We also investigated the distribution of these genes in 17 bifidobacterial strains, including 9 strains, and found that the β-galactosidase genes were present in most bifidobacteria. Homologues of two ABC transporter SBP genes were found in all strains and in some bifidobacteria that are commonly present in the human gut microbiota. These results provide insights into the ability of human-resident bifidobacteria to utilize the main component of GOS in the gastrointestinal tract.

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Keyword(s): ABC transporter , Bifidobacterium breve , galactooligosaccharides (GOS) , galactosyllactose (GL) and prebiotics
© 2017 The Authors
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2017-10-01
2024-04-26
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References

  1. Turroni F, van Sinderen D, Ventura M. Genomics and ecological overview of the genus Bifidobacterium. Int J Food Microbiol 2011; 149:37–44 [View Article][PubMed]
     [Google Scholar]
  2. Schell MA, Karmirantzou M, Snel B, Vilanova D, Berger B et al. The genome sequence of Bifidobacterium longum reflects its adaptation to the human gastrointestinal tract. Proc Natl Acad Sci USA 2002; 99:14422–14427 [View Article][PubMed]
     [Google Scholar]
  3. Parche S, Amon J, Jankovic I, Rezzonico E, Beleut M et al. Sugar transport systems of Bifidobacterium longum NCC2705. J Mol Microbiol Biotechnol 2007; 12:9–19 [View Article][PubMed]
     [Google Scholar]
  4. Sela DA, Chapman J, Adeuya A, Kim JH, Chen F et al. The genome sequence of Bifidobacterium longum subsp. infantis reveals adaptations for milk utilization within the infant microbiome. Proc Natl Acad Sci USA 2008; 105:18964–18969 [View Article][PubMed]
     [Google Scholar]
  5. Enomoto T, Sowa M, Nishimori K, Shimazu S, Yoshida A et al. Effects of bifidobacterial supplementation to pregnant women and infants in the prevention of allergy development in infants and on fecal microbiota. Allergol Int 2014; 63:575–585 [View Article][PubMed]
     [Google Scholar]
  6. Bäckhed F, Ding H, Wang T, Hooper LV, Koh GY et al. The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci USA 2004; 101:15718–15723 [View Article][PubMed]
     [Google Scholar]
  7. Fukuda S, Toh H, Hase K, Oshima K, Nakanishi Y et al. Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature 2011; 469:543–547 [View Article][PubMed]
     [Google Scholar]
  8. Matsuki T, Yahagi K, Mori H, Matsumoto H, Hara T et al. A key genetic factor for fucosyllactose utilization affects infant gut microbiota development. Nat Commun 2016; 7:11939 [View Article][PubMed]
     [Google Scholar]
  9. Krumbeck JA, Maldonado-Gomez MX, Ramer-Tait AE, Hutkins RW. Prebiotics and synbiotics: dietary strategies for improving gut health. Curr Opin Gastroenterol 2016; 32:110–119 [View Article][PubMed]
     [Google Scholar]
  10. Asahara T, Takahashi A, Yuki N, Kaji R, Takahashi T et al. Protective effect of a synbiotic against multidrug-resistant Acinetobacter baumannii in a murine infection model. Antimicrob Agents Chemother 2016; 60:3041–3050 [View Article][PubMed]
     [Google Scholar]
  11. Motoori M, Yano M, Miyata H, Sugimura K, Saito T et al. Randomized study of the effect of synbiotics during neoadjuvant chemotherapy on adverse events in esophageal cancer patients. Clin Nutr 2017; 36:93–99 [View Article][PubMed]
     [Google Scholar]
  12. Hayakawa M, Asahara T, Ishitani T, Okamura A, Nomoto K et al. Synbiotic therapy reduces the pathological gram-negative rods caused by an increased acetic acid concentration in the gut. Dig Dis Sci 2012; 57:2642–2649 [View Article][PubMed]
     [Google Scholar]
  13. Maathuis AJ, van den Heuvel EG, Schoterman MH, Venema K. Galacto-oligosaccharides have prebiotic activity in a dynamic in vitro colon model using a 13C-labeling technique. J Nutr 2012; 142:1205–1212 [View Article][PubMed]
     [Google Scholar]
  14. Matsumoto K, Takada T, Yuki N, Kawakami K, Sakai T et al. Effects of transgalactosylated oligosaccharides mixture (N-GOS) on human intestinal microflora. J Intest Microbiol 2004; 18:25–35
     [Google Scholar]
  15. Sharp R, Fishbain S, Macfarlane GT. Effect of short-chain carbohydrates on human intestinal bifidobacteria and Escherichia coli in vitro. J Med Microbiol 2001; 50:152–160 [View Article][PubMed]
     [Google Scholar]
  16. Walton GE, van den Heuvel EG, Kosters MH, Rastall RA, Tuohy KM et al. A randomised crossover study investigating the effects of galacto-oligosaccharides on the faecal microbiota in men and women over 50 years of age. Br J Nutr 2012; 107:1466–1475 [View Article][PubMed]
     [Google Scholar]
  17. Knol J, Scholtens P, Kafka C, Steenbakkers J, Gro S et al. Colon microflora in infants fed formula with galacto- and fructo-oligosaccharides: more like breast-fed infants. J Pediatr Gastroenterol Nutr 2005; 40:36–42 [View Article][PubMed]
     [Google Scholar]
  18. Sierra C, Bernal MJ, Blasco J, Martínez R, Dalmau J et al. Prebiotic effect during the first year of life in healthy infants fed formula containing GOS as the only prebiotic: a multicentre, randomised, double-blind and placebo-controlled trial. Eur J Nutr 2015; 54:89–99 [View Article][PubMed]
     [Google Scholar]
  19. Holscher HD, Faust KL, Czerkies LA, Litov R, Ziegler EE et al. Effects of prebiotic-containing infant formula on gastrointestinal tolerance and fecal microbiota in a randomized controlled trial. JPEN J Parenter Enteral Nutr 2012; 36:95S–105S [View Article][PubMed]
     [Google Scholar]
  20. Matsuki T, Tajima S, Hara T, Yahagi K, Ogawa E et al. Infant formula with galacto-oligosaccharides (OM55N) stimulates the growth of indigenous bifidobacteria in healthy term infants. Benef Microbes 2016; 7:453–461 [View Article][PubMed]
     [Google Scholar]
  21. Kaneko K, Watanabe Y, Kimura K, Matsumoto K, Mizobuchi T et al. Development of hypoallergenic galacto-oligosaccharides on the basis of allergen analysis. Biosci Biotechnol Biochem 2014; 78:100–108 [View Article][PubMed]
     [Google Scholar]
  22. van Leeuwen SS, Kuipers BJ, Dijkhuizen L, Kamerling JP. Comparative structural characterization of 7 commercial galacto-oligosaccharide (GOS) products. Carbohydr Res 2016; 425:48–58 [View Article][PubMed]
     [Google Scholar]
  23. Shigehisa A, Sotoya H, Sato T, Hara T, Matsumoto H et al. Characterization of a bifidobacterial system that utilizes galacto-oligosaccharides. Microbiology 2015; 161:1463–1470 [View Article][PubMed]
     [Google Scholar]
  24. O'Connell Motherway M, Kinsella M, Fitzgerald GF, van Sinderen D. Transcriptional and functional characterization of genetic elements involved in galacto-oligosaccharide utilization by Bifidobacterium breve UCC2003. Microb Biotechnol 2013; 6:67–79 [View Article][PubMed]
     [Google Scholar]
  25. Andersen JM, Barrangou R, Abou Hachem M, Lahtinen SJ, Goh YJ et al. Transcriptional analysis of oligosaccharide utilization by Bifidobacterium lactis Bl-04. BMC Genomics 2013; 14:312 [View Article][PubMed]
     [Google Scholar]
  26. James K, Motherway MO, Bottacini F, van Sinderen D. Bifidobacterium breve UCC2003 metabolises the human milk oligosaccharides lacto-N-tetraose and lacto-N-neo-tetraose through overlapping, yet distinct pathways. Sci Rep 2016; 6:38560 [View Article][PubMed]
     [Google Scholar]
  27. Viborg AH, Katayama T, Abou Hachem M, Andersen MC, Nishimoto M et al. Distinct substrate specificities of three glycoside hydrolase family 42 β-galactosidases from Bifidobacterium longum subsp. infantis ATCC 15697. Glycobiology 2014; 24:208–216 [View Article][PubMed]
     [Google Scholar]
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Identification of genes involved in galactooligosaccharide utilization in Bifidobacterium breve strain YIT 4014T
Microbiology 163, 1420 (2017); https://doi.org/10.1099/mic.0.000517
/content/journal/micro/10.1099/mic.0.000517
/content/journal/micro/10.1099/mic.0.000517
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