The sialate O-acetylesterase EstA from gut Bacteroidetes species enables sialidase-mediated cross-species foraging of 9-O-acetylated sialoglycans

Journal of Biological Chemistry

Volumn 292, Issue 28, 2017, Pages 11861-11872

  Robinson, Lloyd S ^a   Lewis, Warren G ^a   Lewis, Amanda L ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESCHERICHIA COLI; ESTERS; MAMMALS; POLYSACCHARIDES;

BACTEROIDETES; BIOCHEMICAL STUDIES; CARBON SOURCE; CLOSTRIDIUM DIFFICILE; COLONIC MICROBIOTA; ENZYMATIC DEGRADATION; PATHOGENIC E. COLI; PATHOGENIC MICROBES;

CARBOXYLIC ACIDS;

ACETYLESTERASE; BACTERIAL ENZYME; MUCIN; PROTEIN ESTA; SIALIC ACID; SIALIDASE; SIALOGLYCOPROTEIN; UNCLASSIFIED DRUG; BACTERIAL POLYSACCHARIDE; BACTERIAL PROTEIN; CARBOXYLESTERASE; ESTA PROTEIN, BACTERIA; N ACETYLNEURAMINIC ACID; RECOMBINANT PROTEIN;

ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTEROIDETES; CARBON SOURCE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME SPECIFICITY; ENZYME SUBSTRATE; ESCHERICHIA COLI; FORAGING; IN VITRO STUDY; NONHUMAN; PH; PRIORITY JOURNAL; ACETYLATION; ANIMAL; BACTEROIDES FRAGILIS; BACTEROIDES THETAIOTAOMICRON; BOVINE; ENTEROHEMORRHAGIC ESCHERICHIA COLI; ENZYMOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; HYDROLYSIS; INTESTINE FLORA; INTESTINE MUCOSA; METABOLISM; MICROBIOLOGY; ORGANISMAL INTERACTION; PHYSIOLOGY; STREPTOCOCCUS AGALACTIAE;

ACETYLATION; ANIMALS; BACTERIAL PROTEINS; BACTEROIDES FRAGILIS; BACTEROIDES THETAIOTAOMICRON; BACTEROIDETES; CARBOXYLIC ESTER HYDROLASES; CATTLE; ENTEROHEMORRHAGIC ESCHERICHIA COLI; GASTROINTESTINAL MICROBIOME; HYDROGEN-ION CONCENTRATION; HYDROLYSIS; INTESTINAL MUCOSA; MICROBIAL INTERACTIONS; MUCINS; N-ACETYLNEURAMINIC ACID; NEURAMINIDASE; POLYSACCHARIDES, BACTERIAL; RECOMBINANT PROTEINS; STREPTOCOCCUS AGALACTIAE; SUBSTRATE SPECIFICITY;

EID: 85024399280     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.769232     Document Type: Article

References (77)

1. Johansson, M. E., and Hansson, G. C. (2013) Mucus and the goblet cell. Dig. Dis. 31, 305-309
2. Marcobal, A., Southwick, A. M., Earle, K. A., and Sonnenburg, J. L. (2013) A refined palate: bacterial consumption of host glycans in the gut. Glycobiology 23, 1038-1046
3. Dharmani, P., Srivastava, V., Kissoon-Singh, V., and Chadee, K. (2009) Role of intestinal mucins in innate host defense mechanisms against pathogens. J. Innate. Immun. 1, 123-135
4. Van der Sluis, M., De Koning, B. A., De Bruijn, A. C., Velcich, A., Meijerink, J. P., Van Goudoever, J. B., Büller, H. A., Dekker, J., Van Seuningen, I., Renes, I. B., and Einerhand, A. W. (2006) Muc2-deficient mice spontaneously develop colitis, indicating that muc2 is critical for colonic protection. Gastroenterology 131, 117-129
5. Johansson, M. E., Larsson, J. M., and Hansson, G. C. (2011) The two mucus layers of colon are organized by the Muc2 mucin, whereas the outer layer is a legislator of host-microbial interactions. Proc. Natl. Acad. Sci. U. S. A. 108, 4659-4665
6. Johansson, M. E., Phillipson, M., Petersson, J., Velcich, A., Holm, L., and Hansson, G. C. (2008) The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Proc. Natl. Acad. Sci. U. S. A. 105, 15064-15069
7. Shan, M., Gentile, M., Yeiser, J. R., Walland, A. C., Bornstein, V. U., Chen, K., He, B., Cassis, L., Bigas, A., Cols, M., Comerma, L., Huang, B., Blander, J. M., Xiong, H., Mayer, L., et al. (2013) Mucus enhances gut homeostasis and oral tolerance by delivering immunoregulatory signals. Science 342, 447-453
8. Tailford, L. E., Crost, E. H., Kavanaugh, D., and Juge, N. (2015) Mucin glycan foraging in the human gut microbiome. Front. Genet. 6, 81
9. Faillard, H., and Schauer, R. (1972) Biochim. Biophys. Acta Libr. 5 B, 1246-1267
10. Hoskins, L. C., and Zamcheck, N. (1963) Studies on the "mucous barrier": evaluation of sialic acid as a protective factor against degradation of gastric mucus by pancreatic endopeptidases. Gastroenterology 44, 456-462
11. Hoskins, L. (1981) Human enteric population ecology and degradation of gut mucins. Dig. Dis. Sci. 9, 769-772
12. Angata, T., and Varki, A. (2002) Chemical diversity in the sialic acids and related α-keto acids: an evolutionary perspective. Chem. Rev. 102, 439-469
13. Juge, N., Tailford, L., and Owen, C. D. (2016) Sialidases from gut bacteria: A mini-review. Biochem. Soc. Trans. 44, 166-175
14. Drzeniek, R. (1973) Substrate specificity of neuraminidases. Histochem. J. 5, 271-290
15. Neuberger, A., and Ratcliffe, W. A. (1972) The acid and enzymic hydrolysis of O-acetylated sialic acid residues from rabbit tamm-horsfall glycoprotein. Biochem. J. 129, 683-693
16. Schauer, R., and Faillard, H. (1968) Action specificity of neuraminidase: the action of bacterial neuraminidase on isomeric N, O-diacetylneuraminic acid glycosides in the submaxilllary mucin of horse and cow. Hoppe Seylers Z. Physiol. Chem. 349, 961-968
17. Corfield, A. P., Wagner, S. A., O'Donnell, L. J., Durdey, P., Mountford, R. A., and Clamp, J. R. (1993) The roles of enteric bacterial sialidase, sialate O-acetyl esterase and glycosulfatase in the degradation of human colonic mucin. Glycoconj. J. 10, 72-81
18. Corfield, A. P., Wagner, S. A., Clamp, J. R., Kriaris, M. S., and Hoskins, L. C. (1992) Mucin degradation in the human colon: production of sialidase, sialate O-acetylesterase, N-acetylneuraminate lyase, arylesterase, and glycosulfatase activities by strains of fecal bacteria. Infect. Immun. 60, 3971-3978
19. Faillard, H. (1959) The effect of neuraminidase on different forms of cattle submaxillary mucin. Hoppe Seylers Z. Physiol. Chem. 317, 257-268
20. Corfield, A. P., Williams, A. J., Clamp, J. R., Wagner, S. A., and Mountford, R. A. (1988) Degradation by bacterial enzymes of colonic mucus from normal subjects and patients with inflammatory bowel disease: the role of sialic acid metabolism and the detection of a novel O-acetylsialic acid esterase. Clin. Sci. (Lond.) 74, 71-78
21. Poon, H., Reid, P. E., Ramey, C. W., Dunn, W. L., and Clay, M. G. (1983) Removal of O-acetylated sialic acids from rat colonic epithelial glycoproteins by cell-free extracts of rat faeces. Can. J. Biochem. Cell Biol. 61, 868-874
22. Phansopa, C., Kozak, R. P., Liew, L. P., Frey, A. M., Farmilo, T., Parker, J. L., Kelly, D. J., Emery, R. J., Thomson, R. I., Royle, L., Gardner, R. A., Spencer, D. I., and Stafford, G. P. (2015) Characterization of a sialate-O-acetylesterase (nanS) from the oral pathogen Tannerella forsythia that enhances sialic acid release by nanH, its cognate sialidase. Biochem. J. 472, 157-167
23. Lewis, A. L., Cao, H., Patel, S. K., Diaz, S., Ryan, W., Carlin, A. F., Thon, V., Lewis, W. G., Varki, A., Chen, X., and Nizet, V. (2007) NeuA sialic acid O-acetylesterase activity modulates O-acetylation of capsular polysaccharide in group B Streptococcus. J. Biol. Chem. 282, 27562-27571
24. Steenbergen, S. M., Lee, Y. C., Vann, W. F., Vionnet, J., Wright, L. F., and Vimr, E. R. (2006) Separate pathways for O-acetylation of polymeric and monomeric sialic acids and identification of sialyl O-acetyl esterase in Escherichia coli k1. J. Bacteriol. 188, 6195-6206
25. Steenbergen, S. M., Jirik, J. L., and Vimr, E. R. (2009) Yjhs (nans) is required for Escherichia coli to grow on 9-O-acetylated N-acetylneuraminic acid. J. Bacteriol. 191, 7134-7139
26. Reid, P. E., Culling, C. F., Dunn, W. L., Ramey, C. W., and Clay, M. G. (1975) Differences in chemical composition between the epithelial glycoproteins of the upper and lower halves of rat colon. Can. J. Biochem. 53, 1328-1332
27. Reid, P. E., Culling, C. F., Tsang, W. C., Clay, M. G., Ramey, C. W., and Dunn, W. L. (1975) The demonstration of O-acetylated sialic acids in colonic epithelial glycoproteins. Can. J. Biochem. 53, 388-391
28. Accili, D., Menghi, G., and Gabrielli, M. G. (2008) Lectin histochemistry for in situ profiling of rat colon sialoglycoconjugates. Histol. Histopathol. 23, 863-875
29. Robbe, C., Capon, C., Maes, E., Rousset, M., Zweibaum, A., Zanetta, J. P., and Michalski, J. C. (2003) Evidence of regio-specific glycosylation in human intestinal mucins: presence of an acidic gradient along the intestinal tract. J. Biol. Chem. 278, 46337-46348
30. Rakoff-Nahoum, S., Coyne, M. J., and Comstock, L. E. (2014) An ecological network of polysaccharide utilization among human intestinal symbionts. Curr. Biol. 24, 40-49
31. Ng, K. M., Ferreyra, J. A., Higginbottom, S. K., Lynch, J. B., Kashyap, P. C., Gopinath, S., Naidu, N., Choudhury, B., Weimer, B. C., Monack, D. M., and Sonnenburg, J. L. (2013) Microbiota-liberated host sugars facilitate post-antibiotic expansion of enteric pathogens. Nature 502, 96-99
32. Huang, Y. L., Chassard, C., Hausmann, M., von Itzstein, M., and Hennet, T. (2015) Sialic acid catabolism drives intestinal inflammation and microbial dysbiosis in mice. Nat. Commun. 6, 8141
33. Egan, M., O'Connell Motherway, M., and van Sinderen, D. (2015) A gntrtype transcriptional repressor controls sialic acid utilization in Bifidobacterium breve ucc2003. FEMS Microbiol. Lett. 362, 10.1093/femsle/fnu056
34. Egan, M., Motherway, M. O., Kilcoyne, M., Kane, M., Joshi, L., Ventura, M., and van Sinderen, D. (2014) Cross-feeding by Bifidobacterium breve ucc2003 during co-cultivation with Bifidobacterium bifidum prl2010 in a mucin-based medium. BMC Microbiol. 14, 282
35. Egan, M., O'Connell Motherway, M., Ventura, M., and van Sinderen, D. (2014) Metabolism of sialic acid by Bifidobacterium breve UCC2003. Appl. Environ. Microbiol. 80, 4414-4426
36. Yu, Z. T., Chen, C., and Newburg, D. S. (2013) Utilization of major fucosylated and sialylated human milk oligosaccharides by isolated human gut microbes. Glycobiology 23, 1281-1292
37. Sela, D. A., Li, Y., Lerno, L., Wu, S., Marcobal, A. M., German, J. B., Chen, X., Lebrilla, C. B., and Mills, D. A. (2011) An infant-associated bacterial commensal utilizes breast milk sialyloligosaccharides. J. Biol. Chem. 286, 11909-11918
38. Kiyohara, M., Tanigawa, K., Chaiwangsri, T., Katayama, T., Ashida, H., and Yamamoto, K. (2011) An exo-α-sialidase from Bifidobacteria involved in the degradation of sialyloligosaccharides in human milk and intestinal glycoconjugates. Glycobiology 21, 437-447
39. Nakayama-Imaohji, H., Ichimura, M., Iwasa, T., Okada, N., Ohnishi, Y., and Kuwahara, T. (2012) Characterization of a gene cluster for sialoglycoconjugate utilization in Bacteroides fragilis. J. Med. Invest. 59, 79-94
40. Park, K. H., Kim, M. G., Ahn, H. J., Lee, D. H., Kim, J. H., Kim, Y. W., and Woo, E. J. (2013) Structural and biochemical characterization of the broad substrate specificity of Bacteroides thetaiotaomicron commensal sialidase. Biochim. Biophys. Acta 1834, 1510-1519
41. Marcobal, A., Barboza, M., Sonnenburg, E. D., Pudlo, N., Martens, E. C., Desai, P., Lebrilla, C. B., Weimer, B. C., Mills, D. A., German, J. B., and Sonnenburg, J. L. (2011) Bacteroides in the infant gut consumemilkoligosaccharides? via mucus-utilization pathways. Cell Host Microbe 10, 507-514
42. Vimr, E. R., and Troy, F. A. (1985) Identification of an inducible catabolic system for sialic acids (nan) in Escherichia coli. J. Bacteriol. 164, 845-853
43. Iguchi, A., Thomson, N. R., Ogura, Y., Saunders, D., Ooka, T., Henderson, I. R., Harris, D., Asadulghani, M., Kurokawa, K., Dean, P., Kenny, B., Quail, M. A., Thurston, S., Dougan, G., Hayashi, T., et al. (2009) Complete genome sequence and comparative genome analysis of enteropathogenic Escherichia coli O127:H6 strain e2348/69. J. Bacteriol. 191, 347-354
44. Peris-Bondia, F., Muraille, E., and Van Melderen, L. (2013) Complete genome sequence of the Escherichia coli pmv-1 strain, a model extraintestinal pathogenic E. coli strain used for host-pathogen interaction studies. Genome Announc. 1, e00913-13
45. Reister, M., Hoffmeier, K., Krezdorn, N., Rotter, B., Liang, C., Rund, S., Dandekar, T., Sonnenborn, U., and Oelschlaeger, T. A. (2014) Complete genome sequence of the Gram-negative probiotic Escherichia coli strain nissle 1917. J. Biotechnol. 187, 106-107
46. Schulz, E. C., Schwarzer, D., Frank, M., Stummeyer, K., Mühlenhoff, M., Dickmanns, A., Gerardy-Schahn, R., and Ficner, R. (2010) Structural basis for the recognition and cleavage of polysialic acid by the bacteriophage k1f tailspike protein endoNF. J. Mol. Biol. 397, 341-351
47. Lewis, W. G., Robinson, L. S., Gilbert, N. M., Perry, J. C., and Lewis, A. L. (2013) Degradation, foraging, and depletion of mucus sialoglycans by the vagina-adapted Actinobacterium Gardnerella vaginalis. J. Biol. Chem. 288, 12067-12079
48. Fraser, A. G., and Brown, R. (1981) Neuraminidase production by Bacteroidaceae. J. Med. Microbiol. 14, 63-76
49. Barton, N. W., and Rosenberg, A. (1973) Action of Vibrio cholerae neuraminidase (sialidase) upon the surface of intact cells and their isolated sialolipid components. J. Biol. Chem. 248, 7353-7358
50. Press, A. G., Hauptmann, I. A., Hauptmann, L., Fuchs, B., Fuchs, M., Ewe, K., and Ramadori, G. (1998) Gastrointestinal pH profiles in patients with inflammatory bowel disease. Aliment Pharmacol. Ther. 12, 673-678
51. Bitterman, W., Spencer, R. J., Huizenga, K. A., and Shorter, R. G. (1969) Contact pH of rectal mucosa in humans and dogs. Dis. Colon. Rectum. 12, 96-98
52. Turroni, F., Bottacini, F., Foroni, E., Mulder, I., Kim, J. H., Zomer, A., Sánchez, B., Bidossi, A., Ferrarini, A., Giubellini, V., Delledonne, M., Henrissat, B., Coutinho, P., Oggioni, M., Fitzgerald, G. F., et al. (2010) Genome analysis of bifidobacterium bifidum prl2010 reveals metabolic pathways for host-derived glycan foraging. Proc. Natl. Acad. Sci. U. S. A. 107, 19514-19519
53. Kamerling, J. P., Schauer, R., Shukla, A. K., Stoll, S., Van Halbeek, H., and Vliegenthart, J. F. (1987) Migration of O-acetyl groups in N, O-acetylneuraminic acids. Eur. J. Biochem. 162, 601-607
54. Higa, H. H., Manzi, A., and Varki, A. (1989) O-acetylation and de-Oacetylation of sialic acids. Purification, characterization, and properties of a glycosylated rat liver esterase specific for 9-O-acetylated sialic acids. J. Biol. Chem. 264, 19435-19442
55. Diaz, S., Higa, H. H., Hayes, B. K., and Varki, A. (1989) O-Acetylation and de-O-acetylation of sialic acids: 7- and 9-O-acetylation of α2, 6-linked sialic acids on endogenous N-linked glycans in rat liver golgi vesicles. J. Biol. Chem. 264, 19416-19426
56. Weiman, S., Dahesh, S., Carlin, A. F., Varki, A., Nizet, V., and Lewis, A. L. (2009) Genetic and biochemical modulation of sialic acidO-acetylation on group b streptococcus: phenotypic and functional impact. Glycobiology 19, 1204-1213
57. Lewis, A. L., Nizet, V., and Varki, A. (2004) Discovery and characterization of sialic acid O-acetylation in group b streptococcus. Proc. Natl. Acad. Sci. U. S. A. 101, 11123-11128
58. Lewis, A. L., and Varki, A. (2009) Evolutionary considerations in studying the sialome: Sialic acids and the host-pathogen interface. In Bioinformatics for Glycobiology and Glycomics: An Introduction (von der Lieth, C.-W., Luetteke, T., and Frank, M., eds) pp. 69-88, John Wiley & Sons, Inc., New York
59. Varki, A., and Diaz, S. (1984) The release and purification of sialic acids from glycoconjugates: methods to minimize the loss and migration of O-acetyl groups. Anal. Biochem. 137, 236-247
60. Meyn, L. A., Krohn, M. A., and Hillier, S. L. (2009) Rectal colonization by group B Streptococcus as a predictor of vaginal colonization. Am. J. Obstet. Gynecol. 201, 76.e71-76.e77
61. El Kaoutari, A., Armougom, F., Gordon, J. I., Raoult, D., and Henrissat, B. (2013) The abundance and variety of carbohydrate-active enzymes in the human gut microbiota. Nat. Rev. Microbiol. 11, 497-504
62. Milani, C., Lugli, G. A., Duranti, S., Turroni, F., Mancabelli, L., Ferrario, C., Mangifesta, M., Hevia, A., Viappiani, A., Scholz, M., Arioli, S., Sanchez, B., Lane, J., Ward, D. V., Hickey, R., et al. (2015) Bifidobacteria exhibit social behavior through carbohydrate resource sharing in the gut. Sci. Rep. 5, 15782
63. Comway, T., and Cohen, P. (2015) Commensal and pathogenic Escherichia coli metabolism in the gut. In Metabolism and Bacterial Pathogenesis, pp. 343-362, ASM Press, Washington, D. C.
64. Pudlo, N. A., Urs, K., Kumar, S. S., German, J. B., Mills, D. A., and Martens, E. C. (2015) Symbiotic human gut bacteria with variable metabolic priorities for host mucosal glycans. MBio 6, e01282-e01215
65. Zitomersky, N. L., Atkinson, B. J., Franklin, S. W., Mitchell, P. D., Snapper, S. B., Comstock, L. E., and Bousvaros, A. (2013) Characterization of adherent bacteroidales from intestinal biopsies of children and young adults with inflammatory bowel disease. PLoS One 8, e63686
66. Munyaka, P. M., Rabbi, M. F., Khafipour, E., and Ghia, J. E. (2016) Acute dextran sulfate sodium (DSS)-induced colitis promotes gut microbial dysbiosis in mice. J. Basic Microbiol. 56, 986-998
67. Angelberger, S., Reinisch, W., Makristathis, A., Lichtenberger, C., Dejaco, C., Papay, P., Novacek, G., Trauner, M., Loy, A., and Berry, D. (2013) Temporal bacterial community dynamics vary among ulcerative colitis patients after fecal microbiota transplantation. Am. J. Gastroenterol. 108, 1620-1630
68. Atuma, C., Strugala, V., Allen, A., and Holm, L. (2001) The adherent gastrointestinal mucus gel layer: thickness and physical state in vivo. Am. J. Physiol. Gastrointest. Liver Physiol. 280, G922-G929
69. Johansson, M. E. (2012) Fast renewal of the distal colonic mucus layers by the surface goblet cells as measured by in vivo labeling of mucin glycoproteins. PLoS One 7, e41009
70. Croucher, S. C., Houston, A. P., Bayliss, C. E., and Turner, R. J. (1983) Bacterial populations associated with different regions of the human colon wall. Appl. Environ. Microbiol. 45, 1025-1033
71. Bayliss, C. E., and Turner, R. J. (1982) Examination of organisms associated with mucin in the colon by scanning electron-microscopy. Micron 13, 35-40
72. Hoskins, L. C., and Zamcheck, N. (1968) Bacterial degradation of gastrointestinal mucins. I. Comparison of mucus constituents in the stools of germ-free and conventional rats. Gastroenterology 54, 210-217
73. Rogier, E. W., Frantz, A. L., Bruno, M. E., and Kaetzel, C. S. (2014) Secretory IgA is concentrated in the outer layer of colonic mucus along with gut bacteria. Pathogens 3, 390-403
74. Vaishnava, S., Yamamoto, M., Severson, K. M., Ruhn, K. A., Yu, X., Koren, O., Ley, R., Wakeland, E. K., and Hooper, L. V. (2011) The antibacterial lectin regIIIgamma promotes the spatial segregation of microbiota and host in the intestine. Science 334, 255-258
75. Okumura, R., Kurakawa, T., Nakano, T., Kayama, H., Kinoshita, M., Motooka, D., Gotoh, K., Kimura, T., Kamiyama, N., Kusu, T., Ueda, Y., Wu, H., Iijima, H., Barman, S., Osawa, H., et al. (2016) Lypd8 promotes the segregation of flagellated microbiota and colonic epithelia. Nature 532, 117-121
76. Smith, M. I., Yatsunenko, T., Manary, M. J., Trehan, I., Mkakosya, R., Cheng, J., Kau, A. L., Rich, S. S., Concannon, P., Mychaleckyj, J. C., Liu, J., Houpt, E., Li, J. V., Holmes, E., Nicholson, J., Knights, D., et al. (2013) Gut microbiomes of malawian twin pairs discordant for kwashiorkor. Science 339, 548-554
77. Datsenko, K. A., and Wanner, B. L. (2000) One-step inactivation of chromosomal genes in Escherichia coli k-12 using PCR products. Proc. Natl. Acad. Sci. U. S. A. 97, 6640-6645