Model-driven design of a minimal medium for Akkermansia muciniphila confirms mucus adaptation

Microbial Biotechnology

Volumn 11, Issue 3, 2018, Pages 476-485

  van der Ark, Kees C H ^a   Aalvink, Steven ^a   Suarez Diez, Maria ^a   Schaap, Peter J ^a   de Vos, Willem M ^a,b   Belzer, Clara ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; FRUCTOSE 6 PHOSPHATE; GLUCOSAMINE 6 PHOSPHATE; N ACETYLGLUCOSAMINE; PEPTIDOGLYCAN; PROTEIN GLMS; PROTEIN NAGB; SUGAR PHOSPHATE; UNCLASSIFIED DRUG; MUCIN;

ADAPTATION; AKKERMANSIA MUCINIPHILA; ARTICLE; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIAL METABOLISM; BACTERIUM; CONTROLLED STUDY; NONHUMAN; STOMACH MUCUS; BIOLOGICAL MODEL; CHEMISTRY; CULTURE MEDIUM; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; VERRUCOMICROBIA;

CULTURE MEDIA; HUMANS; METABOLIC NETWORKS AND PATHWAYS; MODELS, BIOLOGICAL; MUCINS; VERRUCOMICROBIA;

EID: 85045465374     PISSN: 17517907     EISSN: 17517915     Source Type: Journal    
DOI: 10.1111/1751-7915.13033     Document Type: Article

References (42)

1. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. (1990) Basic local alignment search tool. J Mol Biol 215: 403–410.
2. Altschul, S.F., Boguski, M.S., Gish, W., and Wootton, J.C. (1994) Issues in searching molecular sequence databases. Nat Genet 6: 119–129.
3. Alvarez-Anorve, L.I., Calcagno, M.L., and Plumbridge, J. (2005) Why does Escherichia coli grow more slowly on glucosamine than on N-acetylglucosamine? Effects of enzyme levels and allosteric activation of GlcN6P deaminase (NagB) on growth rates. J Bacteriol 187: 2974–2982.
4. Alvarez-Anorve, L.I., Gaugue, I., Link, H., Marcos-Viquez, J., Diaz-Jimenez, D.M., Zonszein, S., et al. (2016) Allosteric activation of Escherichia coli glucosamine-6-phosphate deaminase (NagB) in vivo justified by intracellular amino sugar metabolite concentrations. J Bacteriol 198: 1610–1620.
5. Barreteau, H., Kovac, A., Boniface, A., Sova, M., Gobec, S., and Blanot, D. (2008) Cytoplasmic steps of peptidoglycan biosynthesis. FEMS Microbiol Rev 32: 168–207.
6. Bernatchez, S., Szymanski, C.M., Ishiyama, N., Li, J., Jarrell, H.C., Lau, P.C., et al. (2005) A single bifunctional UDP-GlcNAc/Glc 4-epimerase supports the synthesis of three cell surface glycoconjugates in Campylobacter jejuni. J Biol Chem 280: 4792–4802.
7. Burk, D., Lineweaver, H., and Horner, C.K. (1934) The specific influence of acidity on the mechanism of nitrogen fixation by Azotobacter. J Bacteriol 27: 325–340.
8. Calcagno, M., Campos, P.J., Mulliert, G., and Suastegui, J. (1984) Purification, molecular and kinetic properties of glucosamine-6-phosphate isomerase (deaminase) from Escherichia coli. Biochim Biophys Acta 787: 165–173.
9. Caspi, R., Altman, T., Billington, R., Dreher, K., Foerster, H., Fulcher, C.A., et al. (2014) The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases. Nucleic Acids Res 42: D459–D471.
10. Chelliah, V., Juty, N., Ajmera, I., Ali, R., Dumousseau, M., Glont, M., et al. (2015) BioModels: ten-year anniversary. Nucleic Acids Res 43: D542–D548.
11. Derrien, M., Vaughan, E.E., Plugge, C.M., and de Vos, W.M. (2004) Akkermansia muciniphila gen. nov., sp nov., a human intestinal mucin-degrading bacterium. Int J Syst Evol Microbiol 54: 1469–1476.
12. Derrien, M., Collado, M.C., Ben-Amor, K., Salminen, S., and de Vos, W.M. (2008) The Mucin degrader Akkermansia muciniphila is an abundant resident of the human intestinal tract. Appl Environ Microbiol 74: 1646–1648.
13. Derrien, M., Van Baarlen, P., Hooiveld, G., Norin, E., Muller, M., and de Vos, W.M. (2011) Modulation of mucosal immune response, tolerance, and proliferation in mice colonized by the Mucin-degrader Akkermansia muciniphila. Front Microbiol 2: 166.
14. Derrien, M., Belzer, C., and de Vos, W.M. (2016) Akkermansia muciniphila and its role in regulating host functions. Microb Pathog 106: 171–181.
15. Desai, M.S., Seekatz, A.M., Koropatkin, N.M., Kamada, N., Hickey, C.A., Wolter, M., et al. (2016) A dietary fiber-deprived gut microbiota degrades the colonic mucus barrier and enhances pathogen susceptibility. Cell 167(1339–1353): e1321.
16. Durand, P., Golinelli-Pimpaneau, B., Mouilleron, S., Badet, B., and Badet-Denisot, M.A. (2008) Highlights of glucosamine-6P synthase catalysis. Arch Biochem Biophys 474: 302–317.
17. Ebrahim, A., Lerman, J.A., Palsson, B.O., and Hyduke, D.R. (2013) COBRApy: COnstraints-based reconstruction and analysis for python. BMC Syst Biol 7: 74.
18. Everard, A., Belzer, C., Geurts, L., Ouwerkerk, J.P., Druart, C., Bindels, L.B., et al. (2013) Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc Natl Acad Sci USA 110: 9066–9071.
19. Guo, X., Li, S., Zhang, J., Wu, F., Li, X., Wu, D., et al. (2017) Genome sequencing of 39 Akkermansia muciniphila isolates reveals its population structure, genomic and functional diverisity, and global distribution in mammalian gut microbiotas. BMC Genom 18: 800.
20. Gurobi (2016). Optimizer reference manual.
21. 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 USA 108(Suppl 1): 4659–4665.
22. Kadner, R.J., Murphy, G.P., and Stephens, C.M. (1992) Two mechanisms for growth inhibition by elevated transport of sugar phosphates in Escherichia coli. J Gen Microbiol 138: 2007–2014.
23. Kwiatkowska-Semrau, K., Czarnecka, J., Wojciechowski, M., and Milewski, S. (2015) Heterogeneity of quaternary structure of glucosamine-6-phosphate deaminase from Giardia lamblia. Parasitol Res 114: 175–184.
24. Macfarlane, G.T., Cummings, J.H., and Allison, C. (1986) Protein degradation by human intestinal bacteria. J Gen Microbiol 132: 1647–1656.
25. Macfarlane, G.T., Gibson, G.R., and Cummings, J.H. (1992) Comparison of fermentation reactions in different regions of the human colon. J Appl Bacteriol 72: 57–64.
26. Milewski, S. (2002) Glucosamine-6-phosphate synthase–the multi-facets enzyme. Biochim Biophys Acta 1597: 173–192.
27. Muller, T., Walter, B., Wirtz, A., and Burkovski, A. (2006) Ammonium toxicity in bacteria. Curr Microbiol 52: 400–406.
28. Orth, J.D., Thiele, I., and Palsson, B.O. (2010) What is flux balance analysis? Nat Biotechnol 28: 245–248.
29. Ottman, N., Davids, M., Suarez-Diez, M., Boeren, S., Schaap, P.J., Martins Dos Santos, V.A.P., et al. (2017a) Genome-scale model and omics analysis of metabolic capacities of Akkermansia muciniphila reveal a preferential mucin-degrading lifestyle. Appl Environ Microbiol 83: e01014–e01017.
30. Ottman, N., Reunanen, J., Meijerink, M., Pietila, T.E., Kainulainen, V., Klievink, J., et al. (2017b) Pili-like proteins of Akkermansia muciniphila modulate host immune responses and gut barrier function. PLoS ONE 12: e0173004.
31. Ottman, N., Geerlings, S.Y., Aalvink, S., de Vos, W.M., and Belzer, C. (2017) Action and function of Akkermansia muciniphila in microbiome ecology, health and disease. Best Pract Res Clin Gastroenterol [In press] https://doi.org/10.1016/j.bpg.2017.10.001
32. Ouwerkerk, J.P., van der Ark, K.C., Davids, M., Claassens, N.J., Robert Finestra, T., de Vos, W.M., and Belzer, C. (2016) Adaptation of Akkermansia muciniphila to the oxic-anoxic interface of the mucus layer. Appl Environ Microbiol 82: 6983–6993.
33. van Passel, M.W., Kant, R., Zoetendal, E.G., Plugge, C.M., Derrien, M., Malfatti, S.A., et al. (2011) The genome of Akkermansia muciniphila, a dedicated intestinal mucin degrader, and its use in exploring intestinal metagenomes. PLoS ONE 6: e16876.
34. Plovier, H., Everard, A., Druart, C., Depommier, C., Hul, M., Geurts, L., et al. (2017) A purified membrane protein from Akkermansia muciniphila or the pasteurized bacterium improves metabolism in obese and diabetic mice. Nat Med 23: 107–113.
35. Plugge, C.M. (2005) Anoxic media design, preparation, and considerations. Methods Enzymol 397: 3–16.
36. Python (2017) Python Language Reference. Wilmington, DE: Python Software Foundation.
37. Tanaka, T., Takahashi, F., Fukui, T., Fujiwara, S., Atomi, H., and Imanaka, T. (2005) Characterization of a novel glucosamine-6-phosphate deaminase from a hyperthermophilic archaeon. J Bacteriol 187: 7038–7044.
38. Thoden, J.B., Wohlers, T.M., Fridovich-Keil, J.L., and Holden, H.M. (2001) Human UDP-galactose 4-epimerase. Accommodation of UDP-N-acetylglucosamine within the active site. J Biol Chem 276: 15131–15136.
39. Thomsson, K.A., Holmen-Larsson, J.M., Angstrom, J., Johansson, M.E., Xia, L., and Hansson, G.C. (2012) Detailed O-glycomics of the Muc2 mucin from colon of wild-type, core 1- and core 3-transferase-deficient mice highlights differences compared with human MUC2. Glycobiology 22: 1128–1139.
40. Van Herreweghen, F., Van den Abbeele, P., De Mulder, T., De Weirdt, R., Geirnaert, A., Hernandez-Sanabria, E., et al. (2017) In vitro colonisation of the distal colon by Akkermansia muciniphila is largely mucin and pH dependent. Benef Microbes 8: 81–96.
41. Vincent, F., Davies, G.J., and Brannigan, J.A. (2005) Structure and kinetics of a monomeric glucosamine 6-phosphate deaminase: missing link of the NagB superfamily? J Biol Chem 280: 19649–19655.
42. Wu, H.C., and Wu, T.C. (1971) Isolation and characterization of a glucosamine-requiring mutant of Escherichia coli K-12 defective in glucosamine-6-phosphate synthetase. J Bacteriol 105: 455–466.