Bifidobacterium longum subsp. longum exo-β-1,3-galactanase, an enzyme for the degradation of type II arabinogalactan

Applied and Environmental Microbiology

Volumn 80, Issue 15, 2014, Pages 4577-4584

  Fujita, Kiyotaka ^a   Sakaguchi, Takenori ^a   Sakamoto, Ayami ^a   Shimokawa, Michiko ^a   Kitahara, Kanefumi ^a  

^a KAGOSHIMA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; ESCHERICHIA COLI; HYDROLYSIS; POLYSACCHARIDES;

ARABINOGALACTAN; BIFIDOBACTERIUM LONGUM; CARBOHYDRATE SOURCES; DEGRADATIVE ENZYMES; GALACTO-OLIGOSACCHARIDES; GLYCOSIDE HYDROLASE FAMILY 43; HOMOLOGOUS GENES; TRANSCRIPTIONAL ANALYSIS;

ENZYMES;

ARABINOGALACTAN; BACTERIAL PROTEIN; EXO-BETA-(1--3)-D-GALACTANASE; GALACTAN; GLYCOSIDASE;

BIFIDOBACTERIUM; CHEMISTRY; CLASSIFICATION; ENZYME SPECIFICITY; ENZYME STABILITY; ENZYMOLOGY; GENETICS; KINETICS; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; PHYLOGENY; PROTEIN TERTIARY STRUCTURE;

BACTERIAL PROTEINS; BIFIDOBACTERIUM; CLONING, MOLECULAR; ENZYME STABILITY; GALACTANS; GLYCOSIDE HYDROLASES; KINETICS; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTEIN STRUCTURE, TERTIARY; SUBSTRATE SPECIFICITY;

EID: 84904865502     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00802-14     Document Type: Article

References (41)

1. Ichinose H, Yoshida M, Kotake T, Kuno A, Igarashi K, Tsumuraya Y, Samejima M, Hirabayashi J, Kobayashi H, Kaneko S. 2005. An exo-β-1,3-galactanase having a novel β-1,3-galactan-binding module from Phanerochaete chrysosporium. J. Biol. Chem. 280:25820-25829. http://dx.doi.org/10.1074/jbc.M501024200.
2. Tsumuraya Y, Mochizuki N, Hashimoto Y, Kovac P. 1990. Purification of an exo-β-(1→3)-D-galactanase of Irpex lacteus (Polyporus tulipiferae) and its action on arabinogalactan-proteins. J. Biol. Chem. 265:7207-7215.
3. 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. 97:9685-9694. http://dx.doi.org/10.1007/s00253-013-4759-3.
4. Ling NX, Lee J, Ellis M, Liao ML, Mau SL, Guest D, Janssen PH, Kovac P, Bacic A, Pettolino FA. 2012. An exo-β-(1→3)-D-galactanase from Streptomyces sp. provides insights into type II arabinogalactan structure. Carbohydr. Res. 352:70-81. http://dx.doi.org/10.1016/j.carres.2012.02.033.
5. Kotake T, Kitazawa K, Takata R, Okabe K, Ichinose H, Kaneko S, Tsumuraya Y. 2009. Molecular cloning and expression in Pichia pastoris of a Irpex lacteus exo-β-(1→3)-galactanase gene. Biosci. Biotechnol. Biochem. 73:2303-2309. http://dx.doi.org/10.1271/bbb.90433.
6. Ichinose H, Kuno A, Kotake T, Yoshida M, Sakka K, Hirabayashi J, Tsumuraya Y, Kaneko S. 2006. Characterization of an exo-β-1,3-galactanase from Clostridium thermocellum. Appl. Environ. Microbiol. 72: 3515-3523. http://dx.doi.org/10.1128/AEM.72.5.3515-3523.2006.
7. Ichinose H, Kotake T, Tsumuraya Y, Kaneko S. 2006. Characterization of an exo-β-1,3-D-galactanase from Streptomyces avermitilis NBRC14893 acting on arabinogalactan-proteins. Biosci. Biotechnol. Biochem. 70: 2745-2750. http://dx.doi.org/10.1271/bbb.60365.
8. Cassab GI. 1986. Arabinogalactan proteins during the development of soybean root nodules. Planta 168:441-446. http://dx.doi.org/10.1007/BF00392262.
9. Capek P, Matulová M, Navarini L, Suggi-Liverani F. 2010. Structural features of an arabinogalactan-protein isolated from instant coffee powder of Coffea arabica beans. Carbohydr. Polym. 80:180-185. http://dx.doi.org/10.1016/j.carbpol.2009.11.016.
10. Göllner EM, Blaschek W, Classen B. 2010. Structural investigations on arabinogalactan-protein from wheat, isolated with Yariv reagent. J. Agric. Food Chem. 58:3621-3626. http://dx.doi.org/10.1021/jf903843f.
11. Guadalupe Z, Martínez-Pinilla O, Garrido á, Carrillo JD, Ayestarán B. 2012. Quantitative determination of wine polysaccharides by gas chromatography-mass spectrometry (GC-MS) and size exclusion chromatography (SEC). Food Chem. 131:367-374. http://dx.doi.org/10.1016/j.foodchem.2011.08.049.
12. 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. 86:155-160. http://dx.doi.org/10.1104/pp.86.1.155.
13. 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. 100:1269-1275. http://dx.doi.org/10.1017/S0007114508981447.
14. Cherbut C, Michel C, Raison V, Kravtchenko T, Severine M. 2003. Acacia gum is a bifidogenic dietary fiber with high digestive tolerance in healthy humans. Microb. Ecol. Health Dis. 15:43-50. http://dx.doi.org/10.1080/08910600310014377.
15. Crociani F, Alessandrini A, Mucci MM, Biavati B. 1994. Degradation of complex carbohydrates by Bifidobacterium spp. Int. J. Food Microbiol. 24:199-210. http://dx.doi.org/10.1016/0168-1605(94)90119-8.
16. Degnan BA, Macfarlane GT. 1995. Arabinogalactan utilization in continuous cultures of Bifidobacterium longum: effect of co-culture with Bacteroides thetaiotaomicron. Anaerobe 1:103-112. http://dx.doi.org/10.1006/anae.1995.1005.
17. 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. 280:37415-37422. http://dx.doi.org/10.1074/jbc.M506874200.
18. Fujita K, Sakamoto S, Ono Y, Wakao M, Suda Y, Kitahara K, Suganuma T. 2011. Molecular cloning and characterization of a β-Larabinobiosidase in Bifidobacterium longum that belongs to a novel glycoside hydrolase family. J. Biol. Chem. 286:5143-5150. http://dx.doi.org/10.1074/jbc.M110.190512.
19. Ling NX-Y, Pettolino F, Liao M-L, Bacic A. 2009. Preparation of a new chromogenic substrate to assay for β-galactanases that hydrolyse type II arabino-3,6-galactans. Carbohydr. Res. 344:1941-1946. http://dx.doi.org/10.1016/j.carres.2009.07.014.
20. Tsumuraya Y, Hashimoto Y, Yamamoto S, Shibuya N. 1984. Structure of L-arabino-D-galactan-containing glycoproteins from radish leaves. Carbohydr. Res. 134:215-228. http://dx.doi.org/10.1016/0008-6215(84) 85039-9.
21. Sakamoto T, Tanaka H, Nishimura Y, Ishimaru M, Kasai N. 2011. Characterization of an exo-β-1,3-D-galactanase from Sphingomonas sp. 24T and its application to structural analysis of larch wood arabinogalactan. Appl. Environ. Biotechnol. 90:1701-1710. http://dx.doi.org/10.1007/s00253-011-3219-1.
22. Smogyi M. 1952. Notes on sugar determination. J. Biol. Chem. 195: 19-23.
23. Holmes EW, O'Brien JS. 1979. Separation of glycoprotein-derived oligosaccharides by thin-layer chromatography. Anal. Biochem. 93:167-170. http://dx.doi.org/10.1016/S0003-2697(79)80131-1.
24. Yoshimoto M, Yamakawa O, Tanoue H. 2005. Potential chemopreventive properties and varietal difference of dietary fiber from sweetpotato (Ipomoea batatas L.) root. Jpn. Agric. Res. Q. 39:37-43. http://dx.doi.org/10.6090/jarq.39.37.
25. Savard P, Roy D. 2009. Determination of differentially expressed genes involved in arabinoxylan degradation by Bifidobacterium longum NCC2705 using real-time RT-PCR. Probiotics Antimicrob. Proteins 1:121-129. http://dx.doi.org/10.1007/s12602-009-9015-x.
26. 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. 180:447-457. http://dx.doi.org/10.1016/j.jsb.2012.08.005.
27. 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 Hydrocolloids 31:42-48. http://dx.doi.org/10.1016/j.foodhyd.2012.09.014.
28. Ashida H, Miyake A, Kiyohara M, Wada J, Yoshida E, Kumagai H, Katayama T, Yamamoto K. 2009. Two distinct α-L-fucosidases from Bifidobacterium bifidum are essential for the utilization of fucosylated milk oligosaccharides and glycoconjugates. Glycobiology 19:1010-1017. http://dx.doi.org/10.1093/glycob/cwp082.
29. 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: 3996-4004. http://dx.doi.org/10.1128/AEM.00149-08.
30. 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-α-L-fucosidase (AfcA), a novel inverting glycosidase (glycoside hydrolase family 95). J. Bacteriol. 186:4885-4893. http://dx.doi.org/10.1128/JB.186.15.4885-4893.2004.
31. 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. 52:146-163. http://dx.doi.org/10.1002/mnfr.200700121.
32. Abbott DW, Eirin-Lopez JM, Boraston AB. 2008. Insight into ligand diversity and novel biological roles for family 32 carbohydrate-binding modules. Mol. Biol. Evol. 25:155-167. http://dx.doi.org/10.1093/molbev/msm243.
33. González R, Klaassens ES, Malinen E, de Vos WM, Vaughan EE. 2008. Differential transcriptional response of Bifidobacterium longum to human milk, formula milk, and galactooligosaccharide. Appl. Environ. Microbiol. 74:4686-4694. http://dx.doi.org/10.1128/AEM.00122-08.
34. Viborg AH, Katayama T, Hachem MA, Andersen MC, Nishimoto M, Clausen MH, Urashima T, Svensson B, Kitaoka M. 2014. Distinct substrate specificities of three glycoside hydrolase family 42 β-galactosidases from Bifidobacterium longum subsp. infantis ATCC 15697. Glycobiology 24:208-216. http://dx.doi.org/10.1093/glycob/cwt104.
35. Yoshida E, Sakurama H, Kiyohara M, Nakajima M, Kitaoka M, Ashida H, Hirose J, Katayama T, Yamamoto K, Kumagai H. 2012. Bifidobacterium longum subsp. infantis uses two different β-galactosidases for selectively degrading type-1 and type-2 human milk oligosaccharides. Glycobiology 22:361-368. http://dx.doi.org/10.1093/glycob/cwr116.
36. Saishin N, Ueta M, Wada A, Yamamoto I. 2010. Properties of β-galactosidase purified from Bifidobacterium longum subsp. longum JCM 7052 grown on gum arabic. J. Biol. Macromol. 10:23-31.
37. Margolles A, de los Reyes-Gavilan CG. 2003. Purification and functional characterization of a novel α-L-arabinofuranosidase from Bifidobacterium longum B667. Appl. Environ. Microbiol. 69:5096-5103. http://dx.doi.org/10.1128/AEM.69.9.5096-5103.2003.
38. 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. 12:9-19. http://dx.doi.org/10.1159/000096455.
39. Nishimoto M, Kitaoka M. 2007. Identification of N-acetylhexosamine 1-kinase in the complete lacto-N-biose I/galacto-N-biose metabolic pathway in Bifidobacterium longum. Appl. Environ. Microbiol. 73:6444-6449. http://dx.doi.org/10.1128/AEM.01425-07.
40. Fujita K, Takashi Y, Obuchi E, Kitahara K, Suganuma T. 2014. Characterization of a novel β-L-arabinofuranosidase in Bifidobacterium longum: functional elucidation of a DUF1680 protein family member. J. Biol. Chem. 289:5240-5249. http://dx.doi.org/10.1074/jbc.M113.528711.
41. Goodrum LJ, Patel A, Leykam JF, Kieliszewski MJ. 2000. Gum arabic glycoprotein contains glycomodules of both extensin and arabinogalactan-glycoproteins. Phytochemistry 54:99-106. http://dx.doi.org/10.1016/S0031-9422(00)00043-1.