Genetic and biochemical characterization of an oligo-α-1,6-glucosidase from Lactobacillus plantarum

International Journal of Food Microbiology

Volumn 246, Issue , 2017, Pages 32-39

  Delgado, Susana ^a   Flórez, Ana Belén ^a   Guadamuro, Lucía ^a   Mayo, Baltasar ^a  

^a DEPARTMENT OF MICROBIOLOGY AND BIOCHEMISTRY OF DAIRY PRODUCTS   (Spain)

Author keywords

Cloning; Glycosyl hydrolase; Heterologous expression; Lactic acid bacteria; Lactobacillus plantarum; Glucosidase

Indexed keywords

4 NITROPHENYL ALPHA DEXTRO GLUCOPYRANOSIDE; AMINO ACID; AMYLASE; CARBOHYDRATE; GLUCOPYRANOSIDE; GLYCOSIDASE; ISOMALTOSE; PALATINOSE; POLYHISTIDINE TAG; RECOMBINANT PROTEIN; SIGNAL PEPTIDE; UNCLASSIFIED DRUG; 4-NITROPHENYL ALPHA-GLUCOSIDE; ALPHA GLUCOSIDASE; BACTERIAL PROTEIN; GLUCOSIDE; HISTIDINE; MALTOSE; OLIGOSACCHARIDE;

AFFINITY CHROMATOGRAPHY; AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; CYTOPLASM; ENZYME ACTIVE SITE; ENZYME ANALYSIS; ENZYME LOCALIZATION; ENZYME PURIFICATION; ENZYME SPECIFICITY; ESCHERICHIA COLI; GENE IDENTIFICATION; GENE OVEREXPRESSION; GLYCOSYLATION; LACTOBACILLUS PLANTARUM; MOLECULAR CLONING; MOLECULAR WEIGHT; NONHUMAN; OLIGO ALPHA 1,6 GLUCOSIDASE GENE; PHYLOGENETIC TREE; PROTEIN HYDROLYSIS; CHEMISTRY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; KINETICS; LACTOBACILLUS; METABOLISM; NUCLEIC ACID HYBRIDIZATION; PH; PHYLOGENY; PLASMID; PROTEIN TERTIARY STRUCTURE; TEMPERATURE;

ALPHA-AMYLASES; ALPHA-GLUCOSIDASES; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CLONING, MOLECULAR; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, BACTERIAL; GLUCOSIDES; GLYCOSIDE HYDROLASES; GLYCOSYLATION; HISTIDINE; HYDROGEN-ION CONCENTRATION; KINETICS; LACTOBACILLUS; LACTOBACILLUS PLANTARUM; MALTOSE; MOLECULAR WEIGHT; NUCLEIC ACID HYBRIDIZATION; OLIGOSACCHARIDES; PHYLOGENY; PLASMIDS; PROTEIN STRUCTURE, TERTIARY; SUBSTRATE SPECIFICITY; TEMPERATURE;

EID: 85011824658     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2017.01.021     Document Type: Article

References (43)

1. Acebrón, I., Curiel, J.A., de Las Rivas, B., Muñoz, R., Mancheño, J.M., Cloning, production, purification and preliminary crystallographic analysis of a glycosidase from the food lactic acid bacterium Lactobacillus plantarum CECT 748(T). Protein Expr. Purif. 68 (2009), 177–182.
2. Ávila, M., Jaquet, M., Moine, D., Requena, T., Peláez, C., Arigoni, F., Jankovic, I., Physiological and biochemical characterization of the two alpha-L-rhamnosidases of Lactobacillus plantarum NCC245. Microbiology 155 (2009), 2739–2749.
3. Bringel, F., Quenee, P., Tailliez, P., Polyphasic investigation of the diversity within Lactobacillus plantarum related strains revealed two L. plantarum subgroups. Syst. Appl. Microbiol. 24 (2001), 561–571.
4. Davies, G.J., Gloster, T.M., Henrissat, B., Recent structural insights into the expanding world of carbohydrate-active enzymes. Curr. Opin. Struct. Biol. 15 (2005), 637–645.
5. De Cort, S., Shantha Kumara, H.M.C., Verachtert, H., Localization and characterization of α-glucosidase activity in Lactobacillus brevis. Appl. Environ. Microbiol. 60 (1994), 3074–3078.
6. Di Cagno, R., Minervini, G., Sgarbi, E., Lazzi, C., Bernini, V., Neviani, E., Gobbetti, M., Comparison of phenotypic (Biolog System) and genotypic (random amplified polymorphic DNA-polymerase chain reaction, RAPD-PCR, and amplified fragment length polymorphism, AFLP) methods for typing Lactobacillus plantarum isolates from raw vegetables and fruits. Int. J. Food Microbiol. 143 (2010), 246–253.
7. Faijes, M., Planas, A., In vitro synthesis of artificial polysaccharides by glycosidases and glycosynthases. Carbohydr. Res. 342 (2007), 1581–1594.
8. Gänzle, M.G., Follador, R., Metabolism of oligosaccharides and starch in lactobacilli: a review. Front. Microbiol. 3 (2012), 1–15.
9. Garbe, J., Collin, M., Bacterial hydrolysis of host glycoproteins - powerful protein modification and efficient nutrient acquisition. J. Innate Immun. 4 (2012), 121–131.
10. Goffin, D., Delzenne, N., Blecker, C., Hanon, E., Deroanne, C., Paquot, M., Will isomalto-oligosaccharides, a well-established functional food in Asia, break through the European and American market? The status of knowledge on these prebiotics. Crit. Rev. Food Sci. Nutr. 51 (2011), 394–409.
11. Guex, N., Peitsch, M.C., Schwede, T., Automated comparative protein structure modeling with SWISS-MODEL and Swiss-PdbViewer: a historical perspective. Electrophoresis 30 (2009), S162–S173.
12. Henrissat, B., A classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem. J. 280 (1991), 309–316.
13. Henrissat, B., Bairoch, A., Updating the sequence-based classification of glycosyl hydrolases. Biochem. J. 316 (1996), 695–696.
14. Hondoh, H., Saburi, W., Mori, H., Okuyama, M., Nakada, T., Matsuura, Y., Kimura, A., Substrate recognition mechanism of alpha-1,6-glucosidic linkage hydrolyzing enzyme, dextran glucosidase from Streptococcus mutans. J. Mol. Biol. 378 (2008), 913–922.
15. Humblot, C., Turpin, W., Chevalier, F., Picq, C., Rochette, I., Guyot, J.P., Determination of expression and activity of genes involved in starch metabolism in Lactobacillus plantarum A6 during fermentation of a cereal-based gruel. Int. J. Food Microbiol. 185 (2014), 103–111.
16. Iqbal, S., Nguyen, T.H., Nguyen, T.T., Maischberger, T., Haltrich, D., Beta-galactosidase from Lactobacillus plantarum WCFS1: biochemical characterization and formation of prebiotic galacto-oligosaccharides. Carbohydr. Res. 345 (2010), 1408–1416.
17. Kang, M.S., Okuyama, M., Mori, H., Kimura, A., The first alpha-1,3-glucosidase from bacterial origin belonging to glycoside hydrolase family 31. Biochimie 91 (2009), 1434–1442.
18. Kelly, E.D., Bottacini, F., O'Callaghan, J., Motherway, M.O., O'Connell, K.J., Stanton, C., van Sinderen, D., Glycoside hydrolase family 13 α-glucosidases encoded by Bifidobacterium breve UCC2003. A comparative analysis of function, structure and phylogeny. Int. J. Food Microbiol. 224 (2016), 55–65.
19. Kim, J.H., Sunako, M., Ono, H., Murooka, Y., Fukusaki, E., Yamashita, M., Characterization of gene encoding amylopullulanase from plant-originated lactic acid bacterium, Lactobacillus plantarum L137. J. Biosci. Bioeng. 106 (2008), 449–459.
20. Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R., Thompson, J.D., Gibson, T.J., Higgins, D.G., Clustal W and Clustal X version 2.0. Bioinformatics 23 (2007), 2947–2948.
21. LeBlanc, J.G., Garro, M.S., Savoy de Giori, G., Effect of pH on Lactobacillus fermentum growth, raffinose removal, alpha-galactosidase activity and fermentation products. Appl. Microbiol. Biotechnol. 65 (2004), 119–123.
22. Li, K.-B., Chang, K.-Y., Production and properties of α-glucosidase from Lactobacillus acidophilus. Appl. Environ. Microbiol. 46 (1983), 1380–1387.
23. Lina, B.A., Jonker, D., Kozianowski, G., Isomaltulose (Palatinose): a review of biological and toxicological studies. Food Chem. Toxicol. 40 (2002), 1375–1381.
24. Majzlová, K., Pukajová, Z., Janeček, S., Tracing the evolution of the α-amylase subfamily GH13_36 covering the amylolytic enzymes intermediate between oligo-1,6-glucosidases and neopullulanases. Carbohydr. Res. 367 (2013), 48–57.
25. Mayo, B., González, B., Arca, P., Suárez, J.E., Cloning and expression of the plasmid encoded beta-D-galactosidase gene from a Lactobacillus plantarum strain of dairy origin. FEMS Microbiol. Lett. 122 (1994), 145–151.
26. Møller, M.S., Fredslund, F., Majumder, A., Nakai, H., Poulsen, J.C., Lo Leggio, L., Svensson, B., Abou Hachem, M., Enzymology and structure of the GH13_31 glucan 1,6-α-glucosidase that confers isomaltooligosaccharide utilization in the probiotic Lactobacillus acidophilus NCFM. J. Bacteriol. 194 (2012), 4249–4259.
27. Olympia, M., Fukuda, H., Ono, H., Kaneko, Y., Takano, M., Characterization of starch-hydrolyzing lactic acid bacteria isolated from a fermented fish and rice food, “burong bangus”, and its amylolytic enzyme. J. Ferment. Bioeng. 80 (1995), 124–130.
28. Oslancová, A., Janecěk, Š., Oligo-1,6-glucosidase and neopullulanase enzymes subfamilies from α-amylase family defined by the fifth conserved sequence region. CMLS Cell. Mol. Life Sci. 59 (2002), 1945–1959.
29. Pokusaeva, K., O'Connell-Motherway, M., Zomer, A., Fitzgerald, G.F., Sinderen, D., Characterization of two novel alpha-glucosidases from Bifidobacterium breve UCC2003. Appl. Environ. Microbiol. 75 (2009), 1135–1143.
30. Saburi, W., Mori, H., Saito, S., Okuyama, M., Kimura, A., Structural elements in dextran glucosidase responsible for high specificity to long chain substrate. Biochim. Biophys. Acta 1764 (2006), 688–698.
31. Sambrook, J., Russell, D., Molecular Cloning: A Laboratory Manual. third ed., 2001, Cold Spring Harbor Laboratory, Cold Spring Harbor, New York.
32. Saulnier, D.M.A., Molenaar, D., de Vos, W.M., Gibson, G.R., Kolida, S., Identification of prebiotic fructooligosaccharide metabolism in Lactobacillus plantarum WCFS1 trough microarrays. Appl. Environ. Microbiol. 73 (2007), 1753–1765.
33. Siezen, R.J., van Hylckama Vlieg, J.E., Genomic diversity and versatility of Lactobacillus plantarum, a natural metabolic engineer. Microb. Cell Factories, 10, 2011, S3.
34. Siezen, R.J., Tzeneva, V.A., Castioni, A., Wels, M., Phan, H.T., Rademaker, J.L., Starrenburg, M.J., Kleerebezem, M., Molenaar, D., van Hylckama Vlieg, J.E., Phenotypic and genomic diversity of Lactobacillus plantarum strains isolated from various environmental niches. Environ. Microbiol. 12 (2010), 758–773.
35. Silvestroni, A., Connes, C., Sesma, F., De Giori, G.S., Piard, J.C., Characterization of the aglA locus for α-galactosidase in Lactobacillus plantarum. Appl. Environ. Microbiol. 68 (2002), 5464–5471.
36. Spano, G., Rinaldi, A., Ugliano, M., Moio, L., Beneduce, L., Massa, S., A β-glucosidase gene isolated from wine Lactobacillus plantarum is regulated by abiotic stresses. J. Appl. Microbiol. 98 (2005), 855–861.
37. Spear, G.T., McKenna, M., Landay, A.L., Makinde, H., Hamaker, B., French, A.L., Lee, B.H., Effect of pH on cleavage of glycogen by vaginal enzymes. PLoS One, 10, 2015, e0132646.
38. Stam, M.R., Danchin, E.G.J., Rancurel, C., Coutinho, P.M., Henrissat, B., Dividing the large glycoside hydrolase family 13 into subfamilies: towards improved functional annotations of α-amylase-related proteins. Protein Eng. Des. Sel. 19 (2006), 555–562.
39. Suzuki, Y., Oishi, K., Nakano, H., Nagayama, T., A strong correlation between the increase in number of proline residues and the rise in thermostability of five Bacillus oligo-1,6-glucosidases. Appl. Microbiol. Biotechnol. 26 (1987), 546–551.
40. van den Broek, L.A.M., Struijs, K., Verdoes, J.C., Beldman, G., Voragen, A.G.J., Cloning and characterization of α-glucosidases from Bifidobacterium adolescentis DSM 20083. Appl. Microbiol. Biotechnol. 61 (2003), 55–60.
41. van der Maarel, M.J.E.C., Van der Veen, B., Uitdehaag, J.C.M., Leenhuis, H., Dijkhuizen, L., Properties and applications of starch-converting enzymes of the α-amylase family. J. Biotechnol. 94 (2002), 137–155.
42. Watanabe, K., Hata, Y., Kizaki, H., Katsube, Y., Suzuki, Y., The refined crystal structure of Bacillus cereus oligo-1,6-glucosidase at 2.0 Å resolution: structural characterization of proline-substitution sites for protein thermostabilization. J. Mol. Biol. 269 (1997), 142–153.
43. Yamamoto, M., Horikoshi, K., Purification and properties of an oligo-1,6-glucosidase from an alkalophilic Bacillus species. Carbohydr. Res. 197 (1990), 227–235.