Advertisement

Applied Microbiology and Biotechnology

, Volume 103, Issue 3, pp 1299–1310 | Cite as

Degradative enzymes for type II arabinogalactan side chains in Bifidobacterium longum subsp. longum

  • Kiyotaka FujitaEmail author
  • Ayami Sakamoto
  • Satoshi Kaneko
  • Toshihisa Kotake
  • Yoichi Tsumuraya
  • Kanefumi Kitahara
Biotechnologically relevant enzymes and proteins

Abstract

Type II arabinogalactan (AG) is a soluble prebiotic fiber stimulating the proliferation of bifidobacteria in the human gut. Larch AG, which is comprised of type II AG, is known to be utilized as an energy source for Bifidobacterium longum subsp. longum (B. longum). We have previously characterized GH43_24 exo-β-1,3-galactanase (Bl1,3Gal) for the degradation of type II AG main chains in B. longum JCM1217. In this study, we characterized GH30_5 exo-β-1,6-galactobiohydrolase (Bl1,6Gal) and GH43_22 α-l-arabinofuranosidase (BlArafA), which are degradative enzymes for type II AG side chains in cooperation with exo-β-1,3-galactanase. The recombinant exo-β-1,6-galactobiohydrolase specifically released β-1,6-galactobiose (β-1,6-Gal2) from the nonreducing terminal of β-1,6-galactooligosaccharides, and the recombinant α-l-arabinofuranosidase released arabinofuranose (Araf) from α-1,3-Araf-substituted β-1,6-galactooligosaccharides. β-1,6-Gal2 was additively released from larch AG by the combined use of type II AG degradative enzymes, including Bl1,3Gal, Bl1,6Gal, and BlArafA. The gene cluster encoding the type II AG degradative enzymes is conserved in all B. longum strains, but not in other bifidobacterial species. The degradative enzymes for type II AG side chains are thought to be important for the acquisition of type II AG in B. longum.

Keywords

Bifidobacterium longum Type II arabinogalactan Prebiotic Exo-β-1,6-galactobiohydrolase α-l-Arabinofuranosidase 

Notes

Funding

This work was supported in part by JSPS KAKENHI Grant-in-Aid for Scientific Research (C), Grant Number 24580144.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with animals performed by any of the authors.

Supplementary material

253_2018_9566_MOESM1_ESM.pdf (1.2 mb)
ESM 1 (PDF 1199 kb)

References

  1. Aalbers F, Turkenburg JP, Davies GJ, Dijkhuizen L, Lammerts van Bueren A (2015) Structural and functional characterization of a novel family GH115 4-O-methyl-α-glucuronidase with specificity for decorated arabinogalactans. J Mol Biol 427:3935–3946CrossRefGoogle Scholar
  2. Amaretti A, Bernardi T, Leonardi A, Raimondi S, Zanoni S, Rossi M (2013) Fermentation of xylo-oligosaccharides by Bifidobacterium adolescentis DSMZ 18350: kinetics, metabolism, and β-xylosidase activities. Appl Microbiol Biotechnol 97:3109–3117CrossRefGoogle Scholar
  3. Aspeborg H, Coutinho PM, Wang Y, Brumer H, Henrissat B (2012) Evolution, substrate specificity and subfamily classification of glycoside hydrolase family 5 (GH5). BMC Evol Biol 12:186CrossRefGoogle Scholar
  4. Bourgois TM, Van Craeyveld V, Van Campenhout S, Courtin CM, Delcour JA, Robben J, Volckaert G (2007) Recombinant expression and characterization of XynD from Bacillus subtilis subsp. subtilis ATCC 6051: a GH 43 arabinoxylan arabinofuranohydrolase. Appl Microbiol Biotechnol 75:1309–1317CrossRefGoogle Scholar
  5. Brillouet J-M, Williams P, Will F, Müller G, Pellerina P (1996) Structural characterization of an apple juice arabinogalactan-protein which aggregates following enzymic dearabinosylation. Carbohydr Polym 29:271–275CrossRefGoogle Scholar
  6. Calame W, Weseler AR, Viebke C, Flynn C, Siemensma AD (2008) Gum arabic establishes prebiotic functionality in healthy human volunteers in a dose-dependent manner. Br J Nutr 100:1269–1275CrossRefGoogle Scholar
  7. Cartmell A, McKee L, Pena MJ, Larsbrink J, Brumer H, Kaneko S, Ichinose H, Lewis RJ, Vikso-Nielsen A, Gilbert HJ, Marles-Wright J (2011) The structure and function of an arabinan-specific α-1,2-arabinofuranosidase identified from screening the activities of bacterial GH43 glycoside hydrolases. J Biol Chem 286:15483–15495CrossRefGoogle Scholar
  8. Cassab GI (1986) Arabinogalactan proteins during the development of soybean root nodules. Planta 168:441–446CrossRefGoogle Scholar
  9. Crociani F, Alessandrini A, Mucci MM, Biavati B (1994) Degradation of complex carbohydrates by Bifidobacterium spp. Int J Food Microbiol 24:199–210CrossRefGoogle Scholar
  10. Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356CrossRefGoogle Scholar
  11. Ficko-Blean E, Stuart CP, Suits MD, Cid M, Tessier M, Woods RJ, Boraston AB (2012) Carbohydrate recognition by an architecturally complex α-N-acetylglucosaminidase from Clostridium perfringens. PLoS One 7:e33524CrossRefGoogle Scholar
  12. Fujimoto Z, Kuno A, Kaneko S, Kobayashi H, Kusakabe I, Mizuno H (2002) Crystal structures of the sugar complexes of Streptomyces olivaceoviridis E-86 xylanase: sugar binding structure of the family 13 carbohydrate binding module. J Mol Biol 316:65–78CrossRefGoogle Scholar
  13. Fujita K, Oura F, Nagamine N, Katayama T, Hiratake J, Sakata K, Kumagai H, Yamamoto K (2005) Identification and molecular cloning of a novel glycoside hydrolase family of core 1 type O-glycan-specific endo-α-N-acetylgalactosaminidase from Bifidobacterium longum. J Biol Chem 280:37415–37422CrossRefGoogle Scholar
  14. Fujita K, Sakamoto S, Ono Y, Wakao M, Suda Y, Kitahara K, Suganuma T (2011) Molecular cloning and characterization of a β-L-arabinobiosidase in Bifidobacterium longum that belongs to a novel glycoside hydrolase family. J Biol Chem 286:5143–5150CrossRefGoogle Scholar
  15. Fujita K, Sakaguchi T, Sakamoto A, Shimokawa M, Kitahara K (2014a) Bifidobacterium longum subsp. longum exo-β-1,3-galactanase, an enzyme for the degradation of type II arabinogalactan. Appl Environ Microbiol 80:4577–4584CrossRefGoogle Scholar
  16. Fujita K, Takashi Y, Obuchi E, Kitahara K, Suganuma T (2014b) Characterization of a novel β-L-arabinofuranosidase in Bifidobacterium longum: functional elucidation of a DUF1680 protein family member. J Biol Chem 289:5240–5249CrossRefGoogle Scholar
  17. Gavini F, Cayuela C, Antoine J-M, Lecoq C, Lefebvre B, Membré J-M, Neut C (2009) Differences in the distribution of Bifidobacterial and Enterobacterial species in human faecal microflora of three different (children, adults, elderly) age groups. Microb Ecol Health Dis 13:40–45CrossRefGoogle Scholar
  18. Göllner EM, Blaschek W, Classen B (2010) Structural investigations on arabinogalactan-protein from wheat, isolated with Yariv reagent. J Agric Food Chem 58:3621–3626CrossRefGoogle Scholar
  19. Holmes EW, O’Brien JS (1979) Separation of glycoprotein-derived oligosaccharides by thin-layer chromatography. Anal Biochem 93:167–170CrossRefGoogle Scholar
  20. Ichinose H, Kotake T, Tsumuraya Y, Kaneko S (2008a) Characterization of an endo-β-1,6-galactanase from Streptomyces avermitilis NBRC14893. Appl Environ Microbiol 74:2379–2383CrossRefGoogle Scholar
  21. Ichinose H, Yoshida M, Fujimoto Z, Kaneko S (2008b) Characterization of a modular enzyme of exo-1,5-α-L-arabinofuranosidase and arabinan binding module from Streptomyces avermitilis NBRC14893. Appl Microbiol Biotechnol 80:399–408CrossRefGoogle Scholar
  22. Jiang D, Fan J, Wang X, Zhao Y, Huang B, Liu J, Zhang XC (2012) Crystal structure of 1,3Gal43A, an exo-β-1,3-galactanase from Clostridium thermocellum. J Struct Biol 180:447–457CrossRefGoogle Scholar
  23. Kaneko S, Arimoto M, Ohba M, Kobayashi H, Ishii T, Kusakabe I (1998) Purification and substrate specificities of two α-L-arabinofuranosidases from Aspergillus awamori IFO 4033. Appl Environ Microbiol 64:4021–4027Google Scholar
  24. Kato K, Odamaki T, Mitsuyama E, Sugahara H, Xiao JZ, Osawa R (2017) Age-related changes in the composition of gut Bifidobacterium species. Curr Microbiol 74:987–995CrossRefGoogle Scholar
  25. Kawabata Y, Kaneko S, Kusakabe I, Gama Y (1995) Synthesis of regioisomeric methyl α-L-arabinofuranobiosides. Carbohydr Res 267:39–47CrossRefGoogle Scholar
  26. Kelly GS (1999) Larch arabinogalactan: clinical relevance of a novel immune-enhancing polysaccharide. Altern Med Rev 4:96–103Google Scholar
  27. Kotake T, Kaneko S, Kubomoto A, Haque MA, Kobayashi H, Tsumuraya Y (2004) Molecular cloning and expression in Escherichia coli of a Trichoderma viride endo-β-(1→6)-galactanase gene. Biochem J 377:749–755CrossRefGoogle Scholar
  28. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874CrossRefGoogle Scholar
  29. Luonteri E, Laine C, Uusitalo S, Teleman A, Siika-aho M, Tenkanen M (2003) Purification and characterization of Aspergillus β-D-galactanases acting on β-1,4- and β-1,3/6-linked arabinogalactans. Carbohydr Polym 53:155–168CrossRefGoogle Scholar
  30. Mewis K, Lenfant N, Lombard V, Henrissat B (2016) Dividing the large glycoside hydrolase family 43 into subfamilies: a motivation for detailed enzyme characterization. Appl Environ Microbiol 82:1686–1692CrossRefGoogle Scholar
  31. Nie S-P, Wang C, Cui SW, Wang Q, Xie M-Y, Phillips GO (2013) A further amendment to the classical core structure of gum arabic (Acacia senegal). Food Hydrocoll 31:42–48CrossRefGoogle Scholar
  32. Odonmažig P, Ebringerová A, Machová E, Alföldi J (1994) Structural and molecular properties of the arabinogalactan isolated from Mongolian larchwood (Larix dahurica L.). Carbohydr Res 252:317–324CrossRefGoogle Scholar
  33. Okawa M, Fukamachi K, Tanaka H, Sakamoto T (2013) Identification of an exo-β-1,3-D-galactanase from Fusarium oxysporum and the synergistic effect with related enzymes on degradation of type II arabinogalactan. Appl Microbiol Biotechnol 97:9685–9694CrossRefGoogle Scholar
  34. Ozaki S, Oki N, Suzuki S, Kitamura S (2010) Structural characterization and hypoglycemic effects of arabinogalactan-protein from the tuberous cortex of the white-skinned sweet potato (Ipomoea batatas L.). J Agric Food Chem 58:11593–11599CrossRefGoogle Scholar
  35. Parche S, Amon J, Jankovic I, Rezzonico E, Beleut M, Barutçu H, Schendel I, Eddy MP, Burkovski A, Arigoni F, Titgemeyer F (2007) Sugar transport systems of Bifidobacterium longum NCC2705. J Mol Microbiol Biotechnol 12:9–19CrossRefGoogle Scholar
  36. Ponder GR, Richards GN (1997) Arabinogalactan from Western larch, part III: alkaline degradation revisited, with novel conclusions on molecular structure. Carbohydr Polym 34:251–261CrossRefGoogle Scholar
  37. Sakamoto T, Taniguchi Y, Suzuki S, Ihara H, Kawasaki H (2007) Characterization of Fusarium oxysporum β-1,6-galactanase, an enzyme that hydrolyzes larch wood arabinogalactan. Appl Environ Microbiol 73:3109–3112CrossRefGoogle Scholar
  38. Saulnier L, Brillouet J-M, Moutounet M, du Penhoat CH, Michon V (1992) New investigations of the structure of grape arabino-galactan-protein. Carbohydr Res 224:219–235CrossRefGoogle Scholar
  39. Shimoda R, Okabe K, Kotake T, Matsuoka K, Koyama T, Tryfona T, Liang HC, Dupree P, Tsumuraya Y (2014) Enzymatic fragmentation of carbohydrate moieties of radish arabinogalactan-protein and elucidation of the structures. Biosci Biotechnol Biochem 78:818–831CrossRefGoogle Scholar
  40. Shinozaki A, Kawakami T, Hosokawa S, Sakamoto T (2014) A novel GH43 α-L-arabinofuranosidase of Penicillium chrysogenum that preferentially degrades single-substituted arabinosyl side chains in arabinan. Enzym Microb Technol 58-59:80–86CrossRefGoogle Scholar
  41. Shinozaki A, Hosokawa S, Nakazawa M, Ueda M, Sakamoto T (2015) Identification and characterization of three Penicillium chrysogenum α-L-arabinofuranosidases (PcABF43B, PcABF51C, and AFQ1) with different specificities toward arabino-oligosaccharides. Enzym Microb Technol 73-74:65–71CrossRefGoogle Scholar
  42. Smogyi M (1952) Notes on sugar determination. J Biol Chem 195:19–23Google Scholar
  43. St John FJ, González JM, Pozharski E (2010) Consolidation of glycosyl hydrolase family 30: a dual domain 4/7 hydrolase family consisting of two structurally distinct groups. FEBS Lett 584:4435–4441CrossRefGoogle Scholar
  44. Suzuki R, Wada J, Katayama T, Fushinobu S, Wakagi T, Shoun H, Sugimoto H, Tanaka A, Kumagai H, Ashida H, Kitaoka M, Yamamoto K (2008) Structural and thermodynamic analyses of solute-binding protein from Bifidobacterium longum specific for core 1 disaccharide and lacto-N-biose I. J Biol Chem 283:13165–13173CrossRefGoogle Scholar
  45. Takata R, Tokita K, Mori S, Shimoda R, Harada N, Ichinose H, Kaneko S, Igarashi K, Samejima M, Tsumuraya Y, Kotake T (2010) Degradation of carbohydrate moieties of arabinogalactan-proteins by glycoside hydrolases from Neurospora crassa. Carbohydr Res 345:2516–2522CrossRefGoogle Scholar
  46. ter Beek J, Guskov A, Slotboom DJ (2014) Structural diversity of ABC transporters. J Gen Physiol 143:419–435CrossRefGoogle Scholar
  47. Terpend K, Possemiers S, Daguet D, Marzorati M (2013) Arabinogalactan and fructo-oligosaccharides have a different fermentation profile in the Simulator of the Human Intestinal Microbial Ecosystem (SHIME (R)). Environ Microbiol Rep 5:595–603CrossRefGoogle Scholar
  48. Tryfona T, Liang HC, Kotake T, Tsumuraya Y, Stephens E, Dupree P (2012) Structural characterization of Arabidopsis leaf arabinogalactan polysaccharides. Plant Physiol 160:653–666CrossRefGoogle Scholar
  49. Tsumuraya Y, Hashimoto Y, Yamamoto S, Shibuya N (1984) Structure of L-arabino-D-galactan-containing glycoproteins from radish leaves. Carbohydr Res 134:215–228CrossRefGoogle Scholar
  50. Tsumuraya Y, Ogura K, Hashimoto Y, Mukoyama H, Yamamoto S (1988) Arabinogalactan-proteins from primary and mature roots of radish (Raphanus sativus L.). Plant Physiol 86:155–160CrossRefGoogle Scholar
  51. van den Broek LA, Lloyd RM, Beldman G, Verdoes JC, McCleary BV, Voragen AG (2005) Cloning and characterization of arabinoxylan arabinofuranohydrolase-D3 (AXHd3) from Bifidobacterium adolescentis DSM20083. Appl Microbiol Biotechnol 67:641–647CrossRefGoogle Scholar
  52. van den Broek LA, Hinz SW, Beldman G, Vincken JP, Voragen AG (2008) Bifidobacterium carbohydrases—their role in breakdown and synthesis of (potential) prebiotics. Mol Nutr Food Res 52:146–163CrossRefGoogle Scholar
  53. Wada J, Ando T, Kiyohara M, Ashida H, Kitaoka M, Yamaguchi M, Kumagai H, Katayama T, Yamamoto K (2008) Bifidobacterium bifidum lacto-N-biosidase, a critical enzyme for the degradation of human milk oligosaccharides with a type 1 structure. Appl Environ Microbiol 74:3996–4004CrossRefGoogle Scholar
  54. Yang L, Connaris H, Potter JA, Taylor GL (2015) Structural characterization of the carbohydrate-binding module of NanA sialidase, a pneumococcal virulence factor. BMC Struct Biol 15:15CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Kiyotaka Fujita
    • 1
    • 2
    Email author
  • Ayami Sakamoto
    • 1
  • Satoshi Kaneko
    • 3
  • Toshihisa Kotake
    • 4
  • Yoichi Tsumuraya
    • 4
  • Kanefumi Kitahara
    • 1
    • 2
  1. 1.Faculty of AgricultureKagoshima UniversityKagoshimaJapan
  2. 2.The United Graduate School of Agricultural Sciences Kagoshima UniversityKagoshimaJapan
  3. 3.Faculty of AgricultureUniversity of the RyukyusNishiharaJapan
  4. 4.Graduate School of Science and EngineeringSaitama UniversitySaitamaJapan

Personalised recommendations