Improvement of the Transglycosylation Efficiency of a Lacto-N-Biosidase from Bifidobacterium bifidum by Protein Engineering
Source abstract
Abstract
The lacto-N-biosidase LnbB from Bifidobacterium bifidum JCM 1254 was engineered to improve its negligible transglycosylation efficiency with the purpose of enzymatically synthesizing lacto-N-tetraose (LNT; Gal-β1,3-GlcNAc-β1,3-Gal-β1,4-Glc) in one enzymatic step. LNT is a prebiotic human milk oligosaccharide in itself and constitutes the structural core of a range of more complex human milk oligosaccharides as well. Thirteen different LnbB variants were expressed and screened for transglycosylation activity by monitoring transglycosylation product formation using lacto-N-biose 1,2-oxazoline as donor substrate and lactose as acceptor substrate. LNT was the major reaction product, yet careful reaction analysis revealed the formation of three additional LNT isomers, which we identified to have a β1,2-linkage, a β1,6-linkage, and a 1,1-linkage, respectively, between lacto-N-biose (Gal-β1,3-GlcNAc) and lactose. Considering both maximal transglycosylation yield and regioselectivity as well as minimal product hydrolysis, the best variant was LnbB W394H, closely followed by W465H and Y419N. A high transglycosylation yield was also obtained with W394F, yet the substitution of W394 and W465 of the subsite −1 hydrophobic platform in the enzyme with His dramatically impaired the undesirable product hydrolysis as compared to substitution with Phe; the effect was most pronounced for W465. Using p-nitrophenyl-β-lacto-N-bioside as donor substrate manifested W394 as an important target position. The optimization of the substrate concentrations confirmed that high initial substrate concentration and high acceptor-to-donor ratio both favor transglycosylation.
Source: crossref · Quality: baseline
Research context
OpenAlex topics: Infant Nutrition and Health · Glycosylation and Glycoproteins Research · Carbohydrate Chemistry and Synthesis
SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.
Affiliations
Department of Biotechnology and Biomedicine, Technical University of Denmark, Søltofts Plads 221, 2800 Kongens Lyngby, Denmark
DSM Nutritional Products Ltd., Kogle Allé 4, 2970 Hørsholm, Denmark
Funding
Innovation Fund Denmark
References (55)
Show source-provided references
1. An enzyme releasing lacto-N-biose from oligosaccharides10.1073/pnas.89.18.8512 ↗
2. Purification and characterization of an enzyme releasing lacto-N-biose from oligosaccharides with type 1 chain10.1016/S0021-9258(17)46664-6 ↗
3. Bifidobacterium bifidum lacto-N-biosidase, a critical enzyme for the degradation of human milk oligosaccharides with a type 1 structure10.1128/AEM.00149-08 ↗
4. The carbohydrate-active enzymes database (CAZy) in 201310.1093/nar/gkt1178 ↗
5. Molecular insight into evolution of symbiosis between breast-fed infants and a member of the human gut microbiome Bifidobacterium longum10.1016/j.chembiol.2017.03.012 ↗
6. Gaining insight into the catalysis by GH20 lacto-N-biosidase using small molecule inhibitors and structural analysis10.1039/C5CC05494J ↗
7. Crystal structures of a glycoside hydrolase family 20 lacto-N-biosidase from Bifidobacterium bifidum10.1074/jbc.M112.420109 ↗
8. Muschiol, J., Vuillemin, M., Meyer, A.S., and Zeuner, B. (2020). β-N-Acetylhexosaminidases for carbohydrate synthesis via trans-glycosylation. Catalysts, 10.10.3390/catal10040365 ↗
9. Castejón-Vilatersana, M., Faijes, M., and Planas, A. (2021). Transglycosylation activity of engineered Bifidobacterium lacto-N-biosidase mutants at donor subsites for lacto-N-tetraose synthesis. Int. J. Mol. Sci., 22.10.3390/ijms22063230 ↗
10. Detailed comparative analysis of the catalytic mechanisms of β-N-acetylglucosaminidases from families 3 and 20 of glycoside hydrolases10.1021/bi051121k ↗
11. β-N-Acetylhexosaminidases—The wizards of glycosylation10.1007/s00253-019-10065-0 ↗
12. Zeuner, B., Teze, D., Muschiol, J., and Meyer, A.S. (2019). Synthesis of human milk oligosaccharides: Protein engineering strategies for improved enzymatic transglycosylation. Molecules, 24.10.3390/molecules24112033 ↗
13. Systematic review of the concentrations of oligosaccharides in human milk10.1093/nutrit/nux044 ↗
14. Facile enzymatic conversion of lactose into lacto-N-tetraose and lacto-N-neotetraose10.1023/A:1007020219275 ↗
15. Lacto-N-tetraose synthesis by wild-type and glycosynthase variants of the β-N-hexosaminidase from Bifidobacterium bifidum10.1039/C9OB00424F ↗
16. A chemo-enzymatic approach for the synthesis of human milk oligosaccharide backbone structures10.1515/znc-2018-0149 ↗
17. Glycosynthase principle transformed into biocatalytic process technology: Lacto-N-triose II production with engineered exo-hexosaminidase10.1021/acscatal.9b01288 ↗
18. Visnapuu, T., Teze, D., Kjeldsen, C., Lie, A., Duus, J.Ø., André-Miral, C., Pedersen, L.H., Stougaard, P., and Svensson, B. (2020). Identification and characterization of a β-N-acetylhexosaminidase with a biosynthetic activity from the marine bacterium Paraglaciecola hydrolytica S66T. Int. J. Mol. Sci., 21.10.3390/ijms21020417 ↗
19. Advances in enzymatic glycoside synthesis10.1021/acschembio.6b00340 ↗
20. A single point mutation converts GH84 O-GlcNAc hydrolases into phosphorylases: Experimental and theoretical Evidence10.1021/jacs.9b09655 ↗
21. Mutants of Mucor hiemalis endo-β-N-acetylglucosaminidase show enhanced transglycosylation and glycosynthase-like activities10.1074/jbc.M707137200 ↗
22. Synthesis of derivatized chitooligomers using transglycosidases engineered from the fungal GH20 β-N-acetylhexosaminidase10.1002/adsc.201500075 ↗
23. Glycosynthase reaction meets the flow: Continuous synthesis of lacto-N-triose II by engineered β-hexosaminidase immobilized on solid support10.1002/bit.27293 ↗
24. A novel disaccharide substrate having 1,2-oxazoline moiety for detection of transglycosylating activity of endoglycosidases10.1016/S0304-4165(01)00164-7 ↗
25. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega10.1038/msb.2011.75 ↗
26. Rational enzyme design without structural knowledge: A sequence-based approach for efficient generation of transglycosylases10.1002/chem.202100110 ↗
27. Converting a β-N-acetylhexosaminidase into two trans-β-N-acetylhexosaminidases by domain-targeted mutagenesis10.1007/s00253-019-10253-y ↗
28. Loop protein engineering for improved transglycosylation activity of a β-N-acetylhexosaminidase10.1002/cbic.201800181 ↗
29. The EMBL-EBI search and sequence analysis tools APIs in 201910.1093/nar/gkz268 ↗
30. Conserved unique peptide patterns (CUPP) online platform: Peptide-based functional annotation of carbohydrate active enzymes10.1093/nar/gkaa375 ↗
31. LigPlot+: Multiple ligand-protein interaction diagrams for drug discovery10.1021/ci200227u ↗
32. SignalP 5.0 improves signal peptide predictions using deep neural networks10.1038/s41587-019-0036-z ↗
33. Predicting transmembrane protein topology with a hidden Markov model: Application to complete genomes10.1006/jmbi.2000.4315 ↗
34. Hederos, M., Dekany, G., Demko, S., Kovács, I., and Bajza, I. (2012). Manufacture of Lacto-N-Tetraose. (WO2012155916A1).
35. Dekany, G., Agoston, K., Bajza, I., Boutet, J., Bojstrup, M., Fanefjord, M., Pérez, I.F., Hederos, M., Horvath, F., and Kovács-Pénzes, P. (2010). Synthesis of 2’-O-Fucosyllactose. (WO2010115934A1).
36. Pérez Figueroa, I., Horvath, F., Dekany, G., Agoston, K., Agoston, A., Bajza, I., Boutet, J., Hederos, M., Kovács-Pénzes, P., and Kröger, L. (2011). Production of 6’-O-Sialyllactose and Intermediates. (WO2011100979A1).
37. Kovács, I., Bajza, I., Hederos, M., Dekany, G., Demko, S., and Khanzhin, N. (2013). Synthesis of HMO Core Structures. (WO2013044928A1).
38. Chemical modification of lactose. XII. Preparation of O-(2-acetamido-2-deoxy-beta-d-glucopyranosyl)-(1-6)-o-beta-d-galactopyranolsyl-(1-4)-d-glucopyranose (6’-N-acetylglucosaminyllactose)10.1248/cpb.27.2564 ↗
39. Efficient synthesis of sugar oxazolines from inprotected N-acetyl-2-amino sugars by using chloroformamidinium reagent in water10.1021/jo8024708 ↗
40. Substrate specificity and transfucosylation activity of GH29 α-L-fucosidases for enzymatic production of human milk oligosaccharides10.1016/j.nbt.2017.12.002 ↗
41. Cloning and characterization of the gene encoding a novel β-galactosidase from Bacillus circulans10.1271/bbb.61.1270 ↗
42. Purification and properties of recombinant β-galactosidases from Bacillus circulans10.1023/A:1006916222187 ↗
43. Quantification of neutral human milk oligosaccharides by graphitic carbon high-performance liquid chromatography with tandem mass spectrometry10.1016/j.ab.2012.10.003 ↗
44. Semi-rational approach for converting a GH36 α-glycosidase into an α-transglycosidase10.1093/glycob/cwu124 ↗
45. Structure and mechanism of a bacterial β-glucosaminidase having O-GlcNAcase activity10.1038/nsmb1079 ↗
46. Crystallographic evidence for substrate-assisted catalysis in a bacterial β-hexosaminidase10.1074/jbc.M011067200 ↗
47. Chitinases and construction of a hypertransglycosylating mutant10.1021/bi2002532 ↗
48. Characterization of two novel bacterial type A exo-chitobiose hydrolases having C-terminal 5/12-type carbohydrate-binding modules10.1007/s00253-017-8198-4 ↗
49. Unusual nonreducing sugar GlcNAc-beta(1-1)Man-beta formation by beta-N-acetylhexosaminidase from Aspergillus oryzae10.1016/S0040-4039(98)02171-6 ↗
50. Singh, S., Scigelova, M., Vic, G., and Crout, D.H.G. (1996). Glycosidase-catalysed oligosaccharide synthesis of di-, tri- and tetra-saccharides using the N-acetylhexosaminidase from Aspergillus oryzae and the beta-galactosidase from Bacillus circulans. J. Chem. Soc. Perkin Trans. 1, 1921–1926.10.1039/P19960001921 ↗
51. Garcia-Oliva, C., Hoyos, P., Petrásková, L., Kulik, N., Pelantová, H., Cabanillas, A.H., Rumbero, Á., Křen, V., Hernáiz, M.J., and Bojarová, P. (2019). Acceptor specificity of β-N-Acetylhexosaminidase from Talaromyces flavus: A rational explanation. Int. J. Mol. Sci., 20.10.3390/ijms20246181 ↗
52. Enzymic synthesis of 3’-O- and 6’-O-N-acetylglucosaminyl-N-acetyllactosaminide glycosides catalyzed by β-N-acetyl-D-hexosaminidase from Nocardia orientalis10.1016/S0304-4165(96)00152-3 ↗
53. Enzymic synthesis of HexNAc-containing glycosides10.1016/0008-6215(90)84022-M ↗
54. In-depth characterization of prebiotic galactooligosaccharides by a combination of analytical techniques10.1021/jf902549e ↗
55. Methods for improving enzymatic trans-glycosylation for synthesis of human milk oligosaccharide biomimetics10.1021/jf502619p ↗