Engineering of the Bacillus circulans β-Galactosidase Product Specificity

Biochemistry

Volumn 56, Issue 5, 2017, Pages 704-711

  Yin, Huifang ^a   Pijning, Tjaard ^a,b   Meng, Xiangfeng ^a   Dijkhuizen, Lubbert ^a   Van Leeuwen, Sander S ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIOLOGY; BIOCHEMICAL ENGINEERING; MIXTURES; SACCHARIFICATION;

BIOLOGICAL FUNCTIONS; ENZYME ENGINEERING; ENZYME SPECIFICITY; GALACTO-OLIGOSACCHARIDES; HUMAN MILK OLIGOSACCHARIDES; PRODUCT SPECIFICITY; SATURATION MUTAGENESIS; STRUCTURAL COMPLEXITY;

ENZYMES;

BETA GALACTOSIDASE; GALACTOSE OLIGOSACCHARIDE; TRISACCHARIDE; ARGININE; BACTERIAL PROTEIN; GALACTOSE; LACTOSE; OLIGOSACCHARIDE; PREBIOTIC AGENT; RECOMBINANT PROTEIN;

ARTICLE; BACILLUS CIRCULANS; CARBOHYDRATE ANALYSIS; CONTROLLED STUDY; ENZYME ENGINEERING; ENZYME KINETICS; ENZYME SPECIFICITY; ENZYME STRUCTURE; MOLECULAR CLONING; MUTAGENESIS; MUTANT; MUTATION; PRIORITY JOURNAL; SITE SATURATION MUTAGENESIS; WILD TYPE; BACILLUS; BIOSYNTHESIS; CHEMISTRY; ENZYMOLOGY; ESCHERICHIA COLI; GENE EXPRESSION; GENETICS; KINETICS; METABOLISM; MOLECULAR MODEL; PROTEIN ENGINEERING; PROTEIN SECONDARY STRUCTURE; SITE DIRECTED MUTAGENESIS; STRUCTURE ACTIVITY RELATION; SUPPLY AND DISTRIBUTION;

ARGININE; BACILLUS; BACTERIAL PROTEINS; BETA-GALACTOSIDASE; CARBOHYDRATE SEQUENCE; ESCHERICHIA COLI; GALACTOSE; GENE EXPRESSION; KINETICS; LACTOSE; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; OLIGOSACCHARIDES; PREBIOTICS; PROTEIN ENGINEERING; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 85011706105     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/acs.biochem.7b00032     Document Type: Article

References (48)

1. Gibson, G. R. and Roberfroid, M. B. ( 1995 ) Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics J. Nutr. 125, 1401-1412
2. Park, A. R. and Oh, D. K. ( 2010 ) Galacto-oligosaccharide production using microbial β-galactosidase: current state and perspectives Appl. Microbiol. Biotechnol. 85, 1279-1286 10.1007/s00253-009-2356-2
3. Boehm, G., Fanaro, S., Jelinek, J., Stahl, B., and Marini, A. ( 2003 ) Prebiotic concept for infant nutrition Acta Paediatr. 92, 64-67 10.1111/j.1651-2227.2003.tb00648.x
4. Boehm, G., Stahl, B., Jelinek, J., Knol, J., Miniello, V., and Moro, G. E. ( 2005 ) Prebiotic carbohydrates in human milk and formulas Acta Paediatr. 94, 18-21 10.1080/08035320510043493
5. Oozeer, R., van Limpt, K., Ludwig, T., Amor, K. B., Martin, R., Wind, R. D., Boehm, G., and Knol, J. ( 2013 ) Intestinal microbiology in early life: specific prebiotics can have similar functionalities as human-milk oligosaccharides Am. J. Clin. Nutr. 98, 561S-571S 10.3945/ajcn.112.038893
6. Gourbeyre, P., Denery, S., and Bodinier, M. ( 2011 ) Probiotics, prebiotics, and synbiotics: impact on the gut immune system and allergic reactions J. Leukocyte Biol. 89, 685-695 10.1189/jlb.1109753
7. Knol, J., Scholtens, P., Kafka, C., Steenbakkers, J., Groβ, S., Helm, K., Klarczyk, M., Schöpfer, H., Böckler, H.-M., and Wells, J. ( 2005 ) Colon microflora in infants fed formula with galacto-and fructo-oligosaccharides: more like breast-fed infants J. Pediatr. Gastroenterol. Nutr. 40 ( 1 ) 36-42 10.1097/00005176-200501000-00007
8. Monteagudo-Mera, A., Arthur, J. C., Jobin, C., Keku, T., Bruno-Barcena, J. M., and Azcarate-Peril, M. A. ( 2016 ) High purity galacto-oligosaccharides enhance specific Bifidobacterium species and their metabolic activity in the mouse gut microbiome Benefic. Microbes 7, 247-264 10.3920/BM2015.0114
9. Arslanoglu, S., Moro, G. E., Schmitt, J., Tandoi, L., Rizzardi, S., and Boehm, G. ( 2008 ) Early dietary intervention with a mixture of prebiotic oligosaccharides reduces the incidence of allergic manifestations and infections during the first two years of life J. Nutr. 138, 1091-1095
10. Van Hoffen, E., Ruiter, B., Faber, J., M’Rabet, L., Knol, E. F., Stahl, B., Arslanoglu, S., Moro, G., Boehm, G., and Garssen, J. ( 2009 ) A specific mixture of short-chain galacto-oligosaccharides and long-chain fructo-oligosaccharides induces a beneficial immunoglobulin profile in infants at high risk for allergy Allergy 64, 484-487 10.1111/j.1398-9995.2008.01765.x
11. Shoaf, K., Mulvey, G. L., Armstrong, G. D., and Hutkins, R. W. ( 2006 ) Prebiotic galactooligosaccharides reduce adherence of enteropathogenic Escherichia coli to tissue culture cells Infect. Immun. 74, 6920-6928 10.1128/IAI.01030-06
12. Vulevic, J., Drakoularakou, A., Yaqoob, P., Tzortzis, G., and Gibson, G. R. ( 2008 ) Modulation of the fecal microflora profile and immune function by a novel trans-galactooligosaccharide mixture (B-GOS) in healthy elderly volunteers Am. J. Clin. Nutr. 88, 1438-1446
13. Tremaroli, V. and Bäckhed, F. ( 2012 ) Functional interactions between the gut microbiota and host metabolism Nature 489, 242-249 10.1038/nature11552
14. Playne, M. J. and Crittenden, R. G. ( 2009 ) Galacto-oligosaccharides and other products derived from lactose Adv. Dairy Chem. 3, 121-202 10.1007/978-0-387-84865-5_5
15. Sanz, M. L., Sanz, J., and Martínez-Castro, I. ( 2002 ) Characterization of O-trimethylsilyl oximes of disaccharides by gas chromatography-mass spectrometry Chromatographia 56, 617-622 10.1007/BF02497679
16. Yin, H., Bultema, J. B., Dijkhuizen, L., and van Leeuwen, S. S. ( 2017 ) Reaction kinetics and galactooligosaccharide product profiles of the β-galactosidases from Bacillus circulans, Kluyveromyces lactis and Aspergillus oryzae Food Chem. 225, 230 10.1016/j.foodchem.2017.01.030
17. Bultema, J. B., Kuipers, B. J. H., and Dijkhuizen, L. ( 2014 ) Biochemical characterization of mutants in the active site residues of the β-galactosidase enzyme of Bacillus circulans ATCC 31382 FEBS Open Bio 4, 1015-1020 10.1016/j.fob.2014.11.002
18. Juers, D. H., Matthews, B. W., and Huber, R. E. ( 2012 ) LacZ β-galactosidase: structure and function of an enzyme of historical and molecular biological importance Protein Sci. 21, 1792-1807 10.1002/pro.2165
19. Torres, D. P. M., Gonçalves, M. d. P. F., Teixeira, J. A., and Rodrigues, L. R. ( 2010 ) Galacto-oligosaccharides: production, properties, applications, and significance as prebiotics Compr. Rev. Food Sci. Food Saf. 9, 438-454 10.1111/j.1541-4337.2010.00119.x
20. Otieno, D. O. ( 2010 ) Synthesis of β-galactooligosaccharides from lactose using microbial β-galactosidases Compr. Rev. Food Sci. Food Saf. 9, 471-482 10.1111/j.1541-4337.2010.00121.x
21. Gosling, A., Stevens, G. W., Barber, A. R., Kentish, S. E., and Gras, S. L. ( 2010 ) Recent advances refining galactooligosaccharide production from lactose Food Chem. 121, 307-318 10.1016/j.foodchem.2009.12.063
22. Rodriguez-Colinas, B., de Abreu, M. A., Fernandez-Arrojo, L., de Beer, R., Poveda, A., Jimenez-Barbero, J., Haltrich, D., Ballesteros Olmo, A. O., Fernandez-Lobato, M., and Plou, F. J. ( 2011 ) Production of galacto-oligosaccharides by the β-galactosidase from Kluyveromyces lactis: comparative analysis of permeabilized cells versus soluble enzyme J. Agric. Food Chem. 59, 10477-10484 10.1021/jf2022012
23. Urrutia, P., Rodriguez-Colinas, B., Fernandez-Arrojo, L., Ballesteros, A. O., Wilson, L., Plou, F. J., and Illanes, A. ( 2013 ) Detailed analysis of galactooligosaccharides synthesis with β-galactosidase from Aspergillus oryzae J. Agric. Food Chem. 61, 1081-1087 10.1021/jf304354u
24. Yanahira, S., Kobayashi, T., Suguri, T., Nakakoshi, M., Miura, S., Ishikawa, H., and Nakajima, I. ( 1995 ) Formation of oligosaccharides from lactose by Bacillus circulans β-galactosidase Biosci., Biotechnol., Biochem. 59, 1021-1026 10.1271/bbb.59.1021
25. 1H NMR analysis of the lactose/β-galactosidase-derived galacto-oligosaccharide components of Vivinal® GOS up to DP5 Carbohydr. Res. 400, 59-73 10.1016/j.carres.2014.08.012
26. van Leeuwen, S. S., Kuipers, B. J. H., Dijkhuizen, L., and Kamerling, J. P. ( 2016 ) Corrigendum to “1H NMR analysis of the lactose/β-galactosidase-derived galacto-oligosaccharide components of Vivinal® GOS up to DP5” [Carbohydr. Res. 400 (2014) 59-73] Carbohydr. Res. 419, 69-70 10.1016/j.carres.2015.12.004
27. van Leeuwen, S. S., Kuipers, B. J. H., Dijkhuizen, L., and Kamerling, J. P. ( 2016 ) Comparative structural characterization of 7 commercial galacto-oligosaccharide (GOS) products Carbohydr. Res. 425, 48-58 10.1016/j.carres.2016.03.006
28. Sela, D. A. and Mills, D. A. ( 2010 ) Nursing our microbiota: molecular linkages between bifidobacteria and milk oligosaccharides Trends Microbiol. 18, 298-307 10.1016/j.tim.2010.03.008
29. Barile, D. and Rastall, R. A. ( 2013 ) Human milk and related oligosaccharides as prebiotics Curr. Opin. Biotechnol. 24, 214-219 10.1016/j.copbio.2013.01.008
30. Kralj, S., van Geel-Schutten, I. G. H., Faber, E. J., van der Maarel, M. J. E. C., and Dijkhuizen, L. ( 2005 ) Rational transformation of Lactobacillus reuteri 121 reuteransucrase into a dextransucrase Biochemistry 44, 9206-9216 10.1021/bi050447q
31. 940 has a crucial role in the linkage and reaction specificity of the glucansucrase GTF180 of the probiotic bacterium Lactobacillus reuteri 180 J. Biol. Chem. 289, 32773-32782 10.1074/jbc.M114.602524
32. Ishikawa, K., Kataoka, M., Yanamoto, T., Nakabayashi, M., Watanabe, M., Ishihara, S., and Yamaguchi, S. ( 2015 ) Crystal structure of β-galactosidase from Bacillus circulans ATCC 31382 (BgaD) and the construction of the thermophilic mutants FEBS J. 282, 2540-2552 10.1111/febs.13298
33. Singh, A. K., Pluvinage, B., Higgins, M. A., Dalia, A. B., Woodiga, S. A., Flynn, M., Lloyd, A. R., Weiser, J. N., Stubbs, K. A., Boraston, A. B., and King, S. J. ( 2014 ) Unravelling the multiple functions of the architecturally intricate BgaA PLoS Pathog. 10, e1004364 10.1371/journal.ppat.1004364
34. Song, J., Abe, K., Imanaka, H., Imamura, K., Minoda, M., Yamaguchi, S., and Nakanishi, K. ( 2011 ) Causes of the production of multiple forms of β-galactosidase by Bacillus circulans Biosci., Biotechnol., Biochem. 75, 268-278 10.1271/bbb.100574
35. Song, J., Imanaka, H., Imamura, K., Minoda, M., Yamaguchi, S., and Nakanishi, K. ( 2013 ) The discoidin domain of Bacillus circulans β-galactosidase plays an essential role in repressing galactooligosaccharide production Biosci., Biotechnol., Biochem. 77, 73-79 10.1271/bbb.120583
36. n-d-Glcp type Carbohydr. Res. 400, 54-58 10.1016/j.carres.2014.08.011
37. Ceroni, A., Maass, K., Geyer, H., Geyer, R., Dell, A., and Haslam, S. M. ( 2008 ) Glycoworkbench: a tool for the computer-assisted annotation of mass spectra of glycans J. Proteome Res. 7, 1650-1659 10.1021/pr7008252
38. Perez, S. ( 2014 ) Symbolic Representation of Monosaccharides in the Age of Glycobiology, p 1-19, www.Glycopedia.Eu
39. Depeint, F., Tzortzis, G., Vulevic, J., I’Anson, K., and Gibson, G. R. ( 2008 ) Prebiotic evaluation of a novel galactooligosaccharide mixture produced by the enzymatic activity of Bifidobacterium bifidum NCIMB 41171, in healthy humans: a randomized, double-blind, crossover, placebo-controlled intervention study Am. J. Clin. Nutr. 87, 785-791
40. Cardelle-Cobas, A., Corzo, N., Olano, A., Peláez, C., Requena, T., and Ávila, M. ( 2011 ) Galactooligosaccharides derived from lactose and lactulose: influence of structure on Lactobacillus, Streptococcus and Bifidobacterium growth Int. J. Food Microbiol. 149, 81-87 10.1016/j.ijfoodmicro.2011.05.026
41. Li, W., Wang, K., Sun, Y., Ye, H., Hu, B., and Zeng, X. ( 2015 ) Influences of structures of galactooligosaccharides and fructooligosaccharides on the fermentation in vitro by human intestinal microbiota J. Funct. Foods 13, 158-168 10.1016/j.jff.2014.12.044
42. Quin, M. B. and Schmidt-Dannert, C. ( 2011 ) Engineering of biocatalyst from evolution to creation ACS Catal. 1, 1017-1021 10.1021/cs200217t
43. Jørgensen, F., Hansen, O. C., and Stougaard, P. ( 2001 ) High-efficiency synthesis of oligosaccharides with a truncated β-galactosidase from Bifidobacterium bifidum Appl. Microbiol. Biotechnol. 57, 647-652 10.1007/s00253-001-0845-z
44. Hansson, T., Kaper, T., van der Oost, J., de Vos, W. M., and Adlercreutz, P. ( 2001 ) Improved oligosaccharide synthesis by protein engineering of beta-glucosidase CelB from hyperthermophilic Pyrococcus furiosus Biotechnol. Bioeng. 73, 203-210 10.1002/bit.1052
45. Placier, G., Watzlawick, H., Rabiller, C., and Mattes, R. ( 2009 ) Evolved β-galactosidases from Geobacillus stearothermophilus with improved transgalactosylation yield for galacto-oligosaccharide production Appl. Environ. Microbiol. 75, 6312-6321 10.1128/AEM.00714-09
46. Talens-Perales, D., Polaina, J., and Marín-Navarro, J. ( 2016 ) Structural dissection of the active site of Thermotoga maritima β-Galactosidase identifies key residues for transglycosylating activity J. Agric. Food Chem. 64, 2917-2924 10.1021/acs.jafc.6b00222
47. Wu, Y., Yuan, S., Chen, S., Wu, D., Chen, J., and Wu, J. ( 2013 ) Enhancing the production of galacto-oligosaccharides by mutagenesis of Sulfolobus solfataricus β-galactosidase Food Chem. 138, 1588-1595 10.1016/j.foodchem.2012.11.052
48. Tanaka, S., Takahashi, T., Koide, A., Ishihara, S., Koikeda, S., and Koide, S. ( 2015 ) Monobody-mediated alteration of enzyme specificity Nat. Chem. Biol. 11, 762-764 10.1038/nchembio.1896