Oligosaccharides released from milk glycoproteins are selective growth substrates for infant-associated bifidobacteria

Applied and Environmental Microbiology

Volumn 82, Issue 12, 2016, Pages 3622-3630

  Karav, Sercan ^a   Le Parc, Annabelle ^a   Leite Nobrega de Moura Bell, Juliana Maria ^a   Frese, Steven A ^a,b   Kirmiz, Nina ^a   Block, David E ^a   Barile, Daniela ^a   Mills, David A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Evolve Biosystems   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; GLYCOPROTEINS; MAMMALS; MASS SPECTROMETRY; OLIGOSACCHARIDES; SACCHARIFICATION; SUBSTRATES;

BIFIDOBACTERIUM ANIMALIS; BIFIDOBACTERIUM LONGUM; GROWTH SUBSTRATES; HUMAN MILK OLIGOSACCHARIDES; N-ACETYLGLUCOSAMINIDASE; N-LINKED GLYCOPROTEINS; OLIGOSACCHARIDE STRUCTURE; SELECTIVE PROPERTIES;

POLYSACCHARIDES;

BACTERIUM; DIGESTIVE SYSTEM; GROWTH RESPONSE; MICROBIAL COMMUNITY; MILK; NEONATE; NUTRIENT ENRICHMENT; ORGANIC COMPOUND; POLYSACCHARIDE;

BIFIDOBACTERIUM ANIMALIS SUBSP. LACTIS; BIFIDOBACTERIUM LONGUM; BOVINAE;

GLYCOPROTEIN; N ACETYL BETA GLUCOSAMINIDASE; OLIGOSACCHARIDE;

ANIMAL; BIFIDOBACTERIUM; ENZYMOLOGY; GROWTH, DEVELOPMENT AND AGING; HUMAN; INFANT; METABOLISM; MILK;

ANIMALS; BIFIDOBACTERIUM; GLYCOPROTEINS; HUMANS; INFANT; MANNOSYL-GLYCOPROTEIN ENDO-BETA-N-ACETYLGLUCOSAMINIDASE; MILK; OLIGOSACCHARIDES;

EID: 84971472998     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00547-16     Document Type: Article

References (58)

1. Moremen KW, Tiemeyer M, Nairn AV. 2012. Vertebrate protein glycosylation: diversity, synthesis and function. Nat Rev Mol Cell Biol 13:448-462. http://dx.doi.org/10.1038/nrm3383.
2. Van Berkel P, Geerts M, Van Veen H, Kooiman P, Pieper F, De Boer H, Nuijens J. 1995. Glycosylated and unglycosylated human lactoferrins both bind iron and show identical affinities towards human lysozyme and bacterial lipopolysaccharide, but differ in their susceptibilities towards tryptic proteolysis. Biochem J 312:107-114. http://dx.doi.org/10.1042/bj3120107.
3. Stanley P, Cummings RD. 2009. Structures common to different glycans, p 23-36. In Varki A, Cummings RD, Esko JD, Freeze HH, Stanley P, Bertozzi CR, Hart GW, Etzler ME (ed), Essentials of glycobiology, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
4. Robinson LN, Artpradit C, Raman R, Shriver ZH, Ruchirawat M, Sasisekharan R. 2012. Harnessing glycomics technologies: integrating structure with function for glycan characterization. Electrophoresis 33: 797-814. http://dx.doi.org/10.1002/elps.201100231.
5. Collin M, Olsén A. 2001. EndoS, a novel secreted protein from Streptococcus pyogenes with endoglycosidase activity on human IgG. EMBO J 20:3046-3055. http://dx.doi.org/10.1093/emboj/20.12.3046.
6. Muramatsu H, Tachikui H, Ushida H, Song X-J, Qiu Y, Yamamoto S, Muramatsu T. 2001. Molecular cloning and expression of endo-β-Nacetylglucosaminidase D, which acts on the core structure of complex type asparagine-linked oligosaccharides. J Biochem 129:923-928. http://dx.doi.org/10.1093/oxfordjournals.jbchem.a002938.
7. Collin M, Fischetti VA. 2004. A novel secreted endoglycosidase from Enterococcus faecalis with activity on human immunoglobulinGand ribonuclease B. J Biol Chem 279:22558-22570. http://dx.doi.org/10.1074/jbc.M402156200.
8. Garrido D, Nwosu C, Ruiz-Moyano S, Aldredge D, German JB, Lebrilla CB, Mills DA. 2012. Endo-beta-N-acetylglucosaminidases from infant gut-associated bifidobacteria release complex N-glycans from human milk glycoproteins. Mol Cell Proteomics 11:775-785. http://dx.doi.org/10.1074/mcp.M112.018119.
9. Byers HL, Tarelli E, Homer KA, Beighton D. 1999. Sequential deglycosylation and utilization of the N-linked, complex-type glycans of human a1-acid glycoprotein mediates growth of Streptococcus oralis. Glycobiology 9:469-479. http://dx.doi.org/10.1093/glycob/9.5.469.
10. Renzi F, Manfredi P, Mally M, Moes S, Jenö P, Cornelis GR. 2011. The N-glycan glycoprotein deglycosylation complex (Gpd) from Capnocytophaga canimorsus deglycosylates human IgG. PLoS Pathog 7:e1002118. http://dx.doi.org/10.1371/journal.ppat.1002118.
11. Garbe J, Sjögren J, Cosgrave EF, Struwe WB, Bober M, Olin AI, Rudd PM, Collin M. 2014. EndoE from Enterococcus faecalis hydrolyzes the glycans of the biofilm inhibiting protein lactoferrin and mediates growth. PLoS One 9:e91035. http://dx.doi.org/10.1371/journal.pone.0091035.
12. Burnaugh AM, Frantz LJ, King SJ. 2008. Growth of Streptococcus pneumoniae on human glycoconjugates is dependent upon the sequential activity of bacterial exoglycosidases. J Bacteriol 190:221-230. http://dx.doi.org/10.1128/JB.01251-07.
13. Karav S, Parc AL, Moura Bell JM, Rouquie C, Mills DA, Barile D, Block DE. 2015. Kinetic characterization of a novel endo-beta-Nacetylglucosaminidase on concentrated bovine colostrum whey to release bioactive glycans. Enzyme Microb Technol 77:46-53. http://dx.doi.org/10.1016/j.enzmictec.2015.05.007.
14. Martens EC, Roth R, Heuser JE, Gordon JI. 2009. Coordinate regulation of glycan degradation and polysaccharide capsule biosynthesis by a prominent human gut symbiont. J Biol Chem 284:18445-18457. http://dx.doi.org/10.1074/jbc.M109.008094.
15. Sonnenburg JL, Xu J, Leip DD, Chen C-H, Westover BP, Weatherford J, Buhler JD, Gordon JI. 2005. Glycan foraging in vivo by an intestineadapted bacterial symbiont. Science 307:1955-1959. http://dx.doi.org/10.1126/science.1109051.
16. Crost EH, Tailford LE, Le Gall G, Fons M, Henrissat B, Juge N. 2013. Utilisation of mucin glycans by the human gut symbiont Ruminococcus gnavus is strain-dependent. PLoS One 8:e76341. http://dx.doi.org/10.1371/journal.pone.0076341.
17. Kim W-S, Ohashi M, Tanaka T, Kumura H, Kim G-Y, Kwon I-K, Goh J-S, Shimazaki K-I. 2004. Growth-promoting effects of lactoferrin on L. acidophilus and Bifidobacterium spp. Biometals 17:279-283. http://dx.doi.org/10.1023/B:BIOM.0000027705.57430.f1.
18. Hernandez-Hernandez O, Sanz ML, Kolida S, Rastall RA, Moreno FJ. 2011. In vitro fermentation by human gut bacteria of proteolytically digested caseinomacropeptide nonenzymatically glycosylated with prebiotic carbohydrates. J Agric Food Chem 59:11949-11955. http://dx.doi.org/10.1021/jf203576g.
19. Petschow B, Talbott R, Batema R. 1999. Ability of lactoferrin to promote the growth of Bifidobacterium spp. in vitro is independent of receptor binding capacity and iron saturation level. J Med Microbiol 48:541-549. http://dx.doi.org/10.1099/00222615-48-6-541.
20. Wu S, Tao N, German J, Grimm R, Lebrilla C. 2010. Development of an annotated library of neutral human milk oligosaccharides. J Proteome Res 9:4138-4151. http://dx.doi.org/10.1021/pr100362f.
21. Wu S, Grimm R, German JB, Lebrilla CB. 2011. Annotation and structural analysis of sialylated human milk oligosaccharides. J Proteome Res 10:856-868. http://dx.doi.org/10.1021/pr101006u.
22. 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.
23. Kunz C, Rudloff S, Baier W, Klein N, Strobel S. 2000. Oligosaccharides in human milk: structural, functional, and metabolic aspects. Annu Rev Nutr 20:699-722. http://dx.doi.org/10.1146/annurev.nutr.20.1.699.
24. Smilowitz JT, Lebrilla CB, Mills DA, German JB, Freeman SL. 2014. Breast milk oligosaccharides: structure-function relationships in the neonate. Annu Rev Nutr 34:143. http://dx.doi.org/10.1146/annurev-nutr-071813-105721.
25. Ward RE, Niñonuevo M, Mills DA, Lebrilla CB, German JB. 2007. In vitro fermentability of human milk oligosaccharides by several strains of bifidobacteria. Mol Nutr Food Res 51:1398-1405. http://dx.doi.org/10.1002/mnfr.200700150.
26. LoCascio RG, Niñonuevo 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.
27. Asakuma S, Hatakeyama E, Urashima T, Yoshida E, Katayama T, Yamamoto K, Kumagai H, Ashida H, Hirose J, Kitaoka M. 2011. Physiology of consumption of human milk oligosaccharides by infant gut-associated bifidobacteria. J Biol Chem 286:34583-34592. http://dx.doi.org/10.1074/jbc.M111.248138.
28. Ruiz-Moyano S, Totten SM, Garrido DA, Smilowitz JT, German JB, Lebrilla CB, Mills DA. 2013. Variation in consumption of human milk oligosaccharides by infant gut-associated strains of Bifidobacterium breve. Appl Environ Microbiol 79:6040-6049. http://dx.doi.org/10.1128/AEM.01843-13.
29. Underwood MA, Kalanetra KM, Bokulich NA, Lewis ZT, Mirmiran M, Tancredi DJ, Mills DA. 2013. A comparison of two probiotic strains of bifidobacteria in premature infants. J Pediatr 163:1585.e9-1591.e9. http://dx.doi.org/10.1016/j.jpeds.2013.07.017.
30. Marcobal A, Barboza M, Froehlich J, Block D, German J, Lebrilla C, Mills D. 2010. Consumption of human milk oligosaccharides by gutrelated microbes. J Agric Food Chem 58:5334-5340. http://dx.doi.org/10.1021/jf9044205.
31. Sela DA, Garrido D, Lerno L, Wu S, Tan K, Eom H-J, Joachimiak A, Lebrilla CB, Mills DA. 2012. Bifidobacterium longum subsp. infantis ATCC 15697 α-fucosidases are active on fucosylated human milk oligosaccharides. Appl Environ Microbiol 78:795-803. http://dx.doi.org/10.1128/AEM.06762-11.
32. Garrido D, Kim JH, German JB, Raybould HE, Mills DA. 2011. Oligosaccharide binding proteins from Bifidobacterium longum subsp. infantis reveal a preference for host glycans. PLoS One 6:e17315. http://dx.doi.org/10.1371/journal.pone.0017315.
33. 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.
34. Sela DA, Li Y, Lerno L, Wu S, Marcobal AM, German JB, Chen X, Lebrilla CB, Mills DA. 2011. An infant-associated bacterial commensal utilizes breast milk sialyloligosaccharides. J Biol Chem 286:11909-11918. http://dx.doi.org/10.1074/jbc.M110.193359.
35. Garrido D, Ruiz-Moyano S, Mills DA. 2012. Release and utilization of N-acetyl-D-glucosamine from human milk oligosaccharides by Bifidobacterium longum subsp. infantis. Anaerobe 18:430-435. http://dx.doi.org/10.1016/j.anaerobe.2012.04.012.
36. Azuma N, Yamauchi K, Mitsuoka T. 1984. Bifidus growth-promoting activity of a glycomacropeptide derived from human k-casein. Agric Biol Chem 48:2159-2162.
37. Lee H, Garrido D, Mills DA, Barile D. 2014. Hydrolysis of milk gangliosides by infant-gut associated bifidobacteria determined by microfluidic chips and high-resolution mass spectrometry. Electrophoresis 35:1742-1750. http://dx.doi.org/10.1002/elps.201300653.
38. Ruas-Madiedo P, Gueimonde M, Fernández-García M, Clara G, Margolles A. 2008. Mucin degradation by Bifidobacterium strains isolated from the human intestinal microbiota. Appl Environ Microbiol 74:1936-1940. http://dx.doi.org/10.1128/AEM.02509-07.
39. Kiyohara M, Nakatomi T, Kurihara S, Fushinobu S, Suzuki H, Tanaka T, Shoda S-I, Kitaoka M, Katayama T, Yamamoto K. 2012. α-NAcetylgalactosaminidase from infant-associated bifidobacteria belonging to novel glycoside hydrolase family 129 is implicated in alternative mucin degradation pathway. J Biol Chem 287:693-700. http://dx.doi.org/10.1074/jbc.M111.277384.
40. Dallas DC, Martin WF, Strum JS, Zivkovic AM, Smilowitz JT, Underwood MA, Affolter M, Lebrilla CB, German JB. 2011. N-linked glycan profiling of mature human milk by high-performance microfluidic chip liquid chromatography time-of-flight tandem mass spectrometry. J Agric Food Chem 59:4255-4263. http://dx.doi.org/10.1021/jf104681p.
41. Nwosu CC, Aldredge DL, Lee H, Lerno LA, Zivkovic AM, German JB, Lebrilla CB. 2012. Comparison of the human and bovine milk N-glycome via high-performance microfluidic chip liquid chromatography and tandem mass spectrometry. J Proteome Res 11:2912-2924. http://dx.doi.org/10.1021/pr300008u.
42. Tao N, DePeters E, Freeman S, German J, Grimm R, Lebrilla C. 2008. Bovine milk glycome. J Dairy Sci 91:3768-3778. http://dx.doi.org/10.3168/jds.2008-1305.
43. Barile D, Marotta M, Chu C, Mehra R, Grimm R, Lebrilla C, German J. 2010. Neutral and acidic oligosaccharides in Holstein-Friesian colostrum during the first 3 days of lactation measured by high performance liquid chromatography on a microfluidic chip and time-of-flight mass spectrometry. J Dairy Sci 93:3940-3949. http://dx.doi.org/10.3168/jds.2010-3156.
44. Karav S, Bell JM, Le Parc A, Liu Y, Mills DA, Block DE, Barile D. 2015. Characterizing the release of bioactive N-glycans from dairy products by a novel endo-beta-N-acetylglucosaminidase. Biotechnol Prog 31:1331-1339. http://dx.doi.org/10.1002/btpr.2135.
45. Le Parc A, Karav S, Bell JM, Frese SA, Liu Y, Mills DA, Block DE, Barile D. 2015. A novel endo-beta-N-acetylglucosaminidase releases specific Nglycans depending on different reaction conditions. Biotechnol Prog 31: 1323-1330. http://dx.doi.org/10.1002/btpr.2133.
46. Parche S, Beleut M, Rezzonico E, Jacobs D, Arigoni F, Titgemeyer F, Jankovic I. 2006. Lactose-over-glucose preference in Bifidobacterium longum NCC2705: glcP, encoding a glucose transporter, is subject to lactose repression. J Bacteriol 188:1260-1265. http://dx.doi.org/10.1128/JB.188.4.1260-1265.2006.
47. Le Parc A, Dallas DC, Duaut S, Leonil J, Martin P, Barile D. 2014. Characterization of goat milk lactoferrin N-glycans and comparison with the N-glycomes of human and bovine milk. Electrophoresis 35:1560-1570. http://dx.doi.org/10.1002/elps.201300619.
48. Zivkovic AM, Barile D. 2011. Bovine milk as a source of functional oligosaccharides for improving human health. Adv Nutr 2:284-289. http://dx.doi.org/10.3945/an.111.000455.
49. Petschow B, Talbott R, Batema R. 1999. Ability of lactoferrin to promote the growth of Bifidobacterium spp. in vitro is independent of receptor binding capacity and iron saturation level J Med Microbiol 48:541. http://dx.doi.org/10.1099/00222615-48-6-541.
50. Liepke C, Adermann K, Raida M, Mägert HJ, Forssmann WG, Zucht HD. 2002. Human milk provides peptides highly stimulating the growth of bifidobacteria. Eur J Biochem 269:712-718. http://dx.doi.org/10.1046/j.0014-2956.2001.02712.x.
51. Garrido D, Ruiz-Moyano S, Lemay DG, Sela DA, German JB, Mills DA. 2015. Comparative transcriptomics reveals key differences in the response to milk oligosaccharides of infant gut-associated bifidobacteria. Sci Rep 5:13517. http://dx.doi.org/10.1038/srep13517. (Erratum, 5:15311, http://dx.doi.org/10.1038/srep15311.)
52. LoCascio RG, Ninonuevo MR, Freeman SL, Sela DA, Grimm R, Lebrilla CB, Mills DA, German JB. 2007. Glycoprofiling of bifidobacterial consumption of human milk oligosaccharides demonstrates strain specific, preferential consumption of small chain glycans secreted in early human lactation. J Agric Food Chem 55:8914-8919. http://dx.doi.org/10.1021/jf0710480.
53. Turroni F, Bottacini F, Foroni E, Mulder I, Kim J-H, Zomer A, Sánchez B, Bidossi A, Ferrarini A, Giubellini V. 2010. Genome analysis of Bifidobacterium bifidum PRL2010 reveals metabolic pathways for hostderived glycan foraging. Proc Natl Acad Sci U S A 107:19514-19519. http://dx.doi.org/10.1073/pnas.1011100107.
54. Turroni F, Özcan E, Milani C, Mancabelli L, Viappiani A, van Sinderen D, Sela DA, Ventura M. 2015. Glycan cross-feeding activities between bifidobacteria under in vitro conditions. Front Microbiol 6:1030. http://dx.doi.org/10.3389/fmicb.2015.01030.
55. Egan M, Motherway MOC, Kilcoyne M, Kane M, Joshi L, Ventura M, van Sinderen D. 2014. Cross-feeding by Bifidobacterium breve UCC2003 during co-cultivation with Bifidobacterium bifidum PRL2010 in a mucinbased medium. BMC Microbiol 14:1. http://dx.doi.org/10.1186/1471-2180-14-1.
56. Ng KM, Ferreyra JA, Higginbottom SK, Lynch JB, Kashyap PC, Gopinath S, Naidu N, Choudhury B, Weimer BC, Monack DM. 2013. Microbiotaliberated host sugars facilitate post-antibiotic expansion of enteric pathogens. Nature 502:96-99. http://dx.doi.org/10.1038/nature12503.
57. De Leoz MLA, 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.
58. Sakurama H, Kiyohara M, Wada J, Honda Y, Yamaguchi M, Fukiya S, Yokota A, Ashida H, Kumagai H, Kitaoka M. 2013. Lacto-N-biosidase encoded by a novel gene of Bifidobacterium longum subspecies longum shows unique substrate specificity and requires a designated chaperone for its active expression. J Biol Chem 288:25194-25206. http://dx.doi.org/10.1074/jbc.M113.484733.