The extracellular wall-bound β-N-acetylglucosaminidase from Lactobacillus casei is involved in the metabolism of the human milk oligosaccharide lacto-N-triose

Applied and Environmental Microbiology

Volumn 82, Issue 2, 2016, Pages 570-577

  Bidart, Gonzalo N ^a   Rodríguez Díaz, Jesús ^a,b   Yebra, María J ^a  

^a INSTITUTO DE AGROQUÍMICA Y TECNOLOGÍA DE ALIMENTOS CSIC   (Spain)

^b UNIVERSITY OF VALENCIA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYMES; GENE ENCODING; GENES; HYDROLYSIS; METABOLISM; OLIGOSACCHARIDES; PHYSIOLOGY; SACCHARIFICATION;

GROWTH ANALYSIS; HUMAN MILK OLIGOSACCHARIDES; LACTOBACILLUS CASEI; MANNOSE 6 PHOSPHATES; METABOLIC ADAPTATION; N-ACETYLGLUCOSAMINE; N-ACETYLGLUCOSAMINIDASE; PHYSIOLOGICAL ROLES;

ENZYME ACTIVITY;

BACTERIUM; ENZYME ACTIVITY; HYDROLYSIS; METABOLISM; MILK; PHYSIOLOGICAL RESPONSE;

LACTOBACILLUS CASEI;

ACETYLGLUCOSAMINIDASE; BACTERIAL PROTEIN; LACTO-N-TRIOSE I; OLIGOSACCHARIDE; TRISACCHARIDE;

BREAST MILK; CELL WALL; ENZYMOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; LACTOBACILLUS CASEI; METABOLISM; MICROBIOLOGY;

ACETYLGLUCOSAMINIDASE; BACTERIAL PROTEINS; CELL WALL; HUMANS; LACTOBACILLUS CASEI; MILK, HUMAN; OLIGOSACCHARIDES; TRISACCHARIDES;

EID: 84953896577     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02888-15     Document Type: Article

References (34)

1. Bode L. 2012. Human milk oligosaccharides: every baby needs a sugar mama. Glycobiology 22:1147-1162. http://dx.doi.org/10.1093/glycob/cws074.
2. Garrido D, Dallas DC, Mills DA. 2013. Consumption of human milk glycoconjugates by infant-associated bifidobacteria: mechanisms and implications. Microbiology 159:649-664. http://dx.doi.org/10.1099/mic.0.064113-0.
3. Wang M, Li M, Wu S, Lebrilla CB, Chapkin RS, Ivanov I, Donovan SM. 2015. Fecal microbiota composition of breast-fed infants is correlated with human milk oligosaccharides consumed. J Pediatr Gastroenterol Nutr 60:825-833. http://dx.doi.org/10.1097/MPG.0000000000000752.
4. De Leoz ML, Kalanetra KM, Bokulich NA, Strum JS, Underwood MA, German JB, Mills DA, Lebrilla CB. 2015. Human milk glycomics and gut microbial genomics in infant feces show a correlation between human milk oligosaccharides and gut microbiota: a proof-of-concept study. J Proteome Res 14:491-502. http://dx.doi.org/10.1021/pr500759e.
5. Yu ZT, Chen C, Kling DE, Liu B, McCoy JM, Merighi M, Heidtman M, Newburg DS. 2013. The principal fucosylated oligosaccharides of human milk exhibit prebiotic properties on cultured infant microbiota. Glycobiology 23:169-177. http://dx.doi.org/10.1093/glycob/cws138.
6. Li M, Monaco MH, Wang M, Comstock SS, Kuhlenschmidt TB, Fahey GC, Jr, Miller MJ, Kuhlenschmidt MS, Donovan SM. 2014. Human milk oligosaccharides shorten rotavirus-induced diarrhea and modulate piglet mucosal immunity and colonic microbiota. ISME J 8:1609-1620. http://dx.doi.org/10.1038/ismej.2014.10.
7. Martin R, Heilig GH, Zoetendal EG, Smidt H, Rodriguez JM. 2007. Diversity of the Lactobacillus group in breast milk and vagina of healthy women and potential role in the colonization of the infant gut. J Appl Microbiol 103:2638-2644. http://dx.doi.org/10.1111/j.1365-2672.2007.03497.x.
8. Albesharat R, Ehrmann MA, Korakli M, Yazaji S, Vogel RF. 2011. Phenotypic and genotypic analyses of lactic acid bacteria in local fermented food, breast milk and faeces of mothers and their babies. Syst Appl Microbiol 34:148-155. http://dx.doi.org/10.1016/j.syapm.2010.12.001.
9. Turroni F, Peano C, Pass DA, Foroni E, Severgnini M, Claesson MJ, Kerr C, Hourihane J, Murray D, Fuligni F, Gueimonde M, Margolles A, De Bellis G, O'Toole PW, van Sinderen D, Marchesi JR, Ventura M. 2012. Diversity of bifidobacteria within the infant gut microbiota. PLoS One 7:e36957. http://dx.doi.org/10.1371/journal.pone.0036957.
10. Locascio RG, Ninonuevo MR, Kronewitter SR, Freeman SL, German JB, Lebrilla CB, Mills DA. 2009. A versatile and scalable strategy for glycoprofiling bifidobacterial consumption of human milk oligosaccharides. Microb Biotechnol 2:333-342. http://dx.doi.org/10.1111/j.1751-7915.2008.00072.x.
11. LoCascio RG, Desai P, Sela DA, Weimer B, Mills DA. 2010. Broad conservation of milk utilization genes in Bifidobacterium longum subsp. infantis as revealed by comparative genomic hybridization. Appl Environ Microbiol 76:7373-7381. http://dx.doi.org/10.1128/AEM.00675-10.
12. 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.
13. Miwa M, Horimoto T, Kiyohara M, Katayama T, Kitaoka M, Ashida H, Yamamoto K. 2010. Cooperation of beta-galactosidase and beta-Nacetylhexosaminidase from bifidobacteria in assimilation of human milk oligosaccharides with type 2 structure. Glycobiology 20:1402-1409. http://dx.doi.org/10.1093/glycob/cwq101.
14. Jiang YL, Yu WL, Zhang JW, Frolet C, Di Guilmi AM, Zhou CZ, Vernet T, Chen Y. 2011. Structural basis for the substrate specificity of a novel beta-N-acetylhexosaminidase StrH protein from Streptococcus pneumoniae R6. J Biol Chem 286:43004-43012. http://dx.doi.org/10.1074/jbc. M111.256578.
15. Thi NN, Offen WA, Shareck F, Davies GJ, Doucet N. 2014. Structure and activity of the Streptomyces coelicolor A3(2) beta-N-acetylhexosaminidase provides further insight into GH20 family catalysis and inhibition. Biochemistry 53:1789-1800. http://dx.doi.org/10.1021/bi401697j.
16. Rodriguez-Diaz J, Monedero V, Yebra MJ. 2011. Utilization of natural fucosylated oligosaccharides by three novel alpha-L-fucosidases from a probiotic Lactobacillus casei strain. Appl Environ Microbiol 77:703-705. http://dx.doi.org/10.1128/AEM.01906-10.
17. Rodriguez-Diaz J, Rubio-del-Campo A, Yebra MJ. 2012. Lactobacillus casei ferments the N-acetylglucosamine moiety of fucosyl-alpha-1,3-Nacetylglucosamine and excretes L-fucose. Appl Environ Microbiol 78: 4613-4619. http://dx.doi.org/10.1128/AEM.00474-12.
18. Bidart GN, Rodriguez-Diaz J, Monedero V, Yebra MJ. 2014. A unique gene cluster for the utilization of the mucosal and human milk-associated glycans galacto-N-biose and lacto-N-biose in Lactobacillus casei. Mol Microbiol 93:521-538. http://dx.doi.org/10.1111/mmi.12678.
19. Senba M, Kashige N, Nakashima Y, Miake F, Watanabe K. 2000. Cloning of the gene of beta-N-acetylglucosaminidase from Lactobacillus casei ATCC 27092 and characterization of the enzyme expressed in Escherichia coli. Biol Pharm Bull 23:527-531. http://dx.doi.org/10.1248/bpb.23.527.
20. Leloup L, Ehrlich SD, Zagorec M, Morel-Deville F. 1997. Singlecrossover integration in the Lactobacillus sake chromosome and insertional inactivation of the ptsI and lacL genes. Appl Environ Microbiol 63:2117-2123.
21. Posno M, Leer RJ, van Luijk N, van Giezen MJ, Heuvelmans PT, Lokman BC, Pouwels PH. 1991. Incompatibility of Lactobacillus vectors with replicons derived from small cryptic Lactobacillus plasmids and segregational instability of the introduced vectors. Appl Environ Microbiol 57:1822-1828.
22. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
23. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J Mol Biol 215:403-410. http://dx.doi.org/10.1016/S0022-2836(05)80360-2.
24. Gill JF, Deretic V, Chakrabarty AM. 1986. Overproduction and assay of Pseudomonas aeruginosa phosphomannose isomerase. J Bacteriol 167: 611-615.
25. Marchler-Bauer A, Derbyshire MK, Gonzales NR, Lu S, Chitsaz F, Geer LY, Geer RC, He J, Gwadz M, Hurwitz DI, Lanczycki CJ, Lu F, Marchler GH, Song JS, Thanki N, Wang Z, Yamashita RA, Zhang D, Zheng C, Bryant SH. 2015. CDD: NCBI's Conserved Domain Database. Nucleic Acids Res 43:D222-D226. http://dx.doi.org/10.1093/nar/gku1221.
26. Munoz-Provencio D, Rodriguez-Diaz J, Collado MC, Langella P, Bermudez-Humaran LG, Monedero V. 2012. Functional analysis of the Lactobacillus casei BL23 sortases. Appl Environ Microbiol 78:8684-8693. http://dx.doi.org/10.1128/AEM.02287-12.
27. Monedero V, Gosalbes MJ, Perez-Martinez G. 1997. Catabolite repression in Lactobacillus casei ATCC 393 is mediated by CcpA. J Bacteriol 179:6657-6664.
28. Viana R, Monedero V, Dossonnet V, Vadeboncoeur C, Perez-Martinez G, Deutscher J. 2000. Enzyme I and HPr from Lactobacillus casei: their role in sugar transport, carbon catabolite repression and inducer exclusion. Mol Microbiol 36:570-584.
29. Gosalbes MJ, Monedero V, Alpert CA, Perez-Martinez G. 1997. Establishing a model to study the regulation of the lactose operon in Lactobacillus casei. FEMS Microbiol Lett 148:83-89. http://dx.doi.org/10.1111/j.1574-6968.1997.tb10271.x.
30. Sato Y, Yamamoto Y, Kizaki H, Kuramitsu HK. 1993. Isolation and sequence analysis of the pmi gene encoding phosphomannose isomerase of Streptococcus mutans. FEMS Microbiol Lett 114:61-66. http://dx.doi.org/10.1111/j.1574-6968.1993.tb06551.x.
31. Yeom SJ, Ji JH, Kim NH, Park CS, Oh DK. 2009. Substrate specificity of a mannose-6-phosphate isomerase from Bacillus subtilis and its application in the production of L-ribose. Appl Environ Microbiol 75:4705-4710. http://dx.doi.org/10.1128/AEM.00310-09.
32. Maze A, Boel G, Zuniga M, Bourand A, Loux V, Yebra MJ, Monedero V, Correia K, Jacques N, Beaufils S, Poncet S, Joyet P, Milohanic E, Casaregola S, Auffray Y, Perez-Martinez G, Gibrat JF, Zagorec M, Francke C, Hartke A, Deutscher J. 2010. Complete genome sequence of the probiotic Lactobacillus casei strain BL23. J Bacteriol 192:2647-2648. http://dx.doi.org/10.1128/JB.00076-10.
33. Turroni F, Ventura M, Butto LF, Duranti S, O'Toole PW, Motherway MO, van Sinderen D. 2014. Molecular dialogue between the human gut microbiota and the host: a Lactobacillus and Bifidobacterium perspective. Cell Mol Life Sci 71:183-203. http://dx.doi.org/10.1007/s00018-013-1318-0.
34. Dale GE, Schonfeld HJ, Langen H, Stieger M. 1994. Increased solubility of trimethoprim-resistant type S1 DHFR from Staphylococcus aureus in Escherichia coli cells overproducing the chaperonins GroEL and GroES. Protein Eng 7:925-931. http://dx.doi.org/10.1093/protein/7.7.925.