Skip to main content
SpringerLink
Log in

Protein O-glucosylation in Lactobacillus buchneri

  • Published:
Glycoconjugate Journal Aims and scope Submit manuscript

Abstract

Based on the previous demonstration of surface (S-) layer protein glycosylation in Lactobacillus buchneri 41021/251 and because of general advantages of lactic acid bacteria for applied research, protein glycosylation in this bacterial species was investigated in detail. The cell surface of L. buchneri CD034 is completely covered with an oblique 2D crystalline array (lattice parameters, a = 5.9 nm; b = 6.2 nm; γ ~ 77°) formed by self-assembly of the S-layer protein SlpB. Biochemical and mass spectrometric analyses revealed that SlpB is the most abundant protein and that it is O-glycosylated at four serine residues within the sequence S152-A-S154-S155-A-S157 with, on average, seven Glc(α1-6) residues, each. Subcellular fractionation of strain CD034 indicated a sequential order of SlpB export and glucosylation as evidenced by lack of glucosylation of cytosolic SlpB. Protein glycosylation analysis was extended to strain L. buchneri NRRL B-30929 where an analogous glucosylation scenario could be detected, with the S-layer glycoprotein SlpN containing an O-glycosylation motif identical to that of SlpB. This corroborates previous data on S-layer protein glucosylation of strain 41021/251 and let us propose a species-wide S-layer protein O-glucosylation in L. buchneri targeted at the sequence motif S-A-S-S-A-S. Search of the L. buchneri genomes for the said glucosylation motif revealed one further ORF, encoding the putative glycosyl‐hydrolase LbGH25B and LbGH25N in L. buchneri CD034 and NRRL B-30929, respectively, for which we have indications of a glycosylation comparable to that of the S-layer proteins. These findings demonstrate the presence of a distinct protein O-glucosylation system in Gram-positive and beneficial microbes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

SlpB:

S-layer protein of L. buchneri CD034

SlpN:

S-layer protein of L. buchneri NRRL B-30929

LbGH25B:

Glycosyl‐hydrolase of L. buchneri CD034

LbGH25N:

Glycosyl‐hydrolase of L. buchneri NRRL B-30929

References

  1. Varki, A., Cummings, R.D., Esko, J.D., Freeze, H.H., Stanley, P., Bertozzi, C.R., Hart, G.W., Etzler, M.E.: Essentials of glycobiology, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Habor (2009). 484 pages

    Google Scholar 

  2. Upreti, R.K., Kumar, M., Shankar, V.: Bacterial glycoproteins: functions, biosynthesis and applications. Proteomics 3, 363–379 (2003)

    Article  CAS  PubMed  Google Scholar 

  3. Schmidt, M.A., Riley, L.W., Benz, I.: Sweet new world: glycoproteins in bacterial pathogens. Trends Microbiol. 11, 554–561 (2003)

    Article  CAS  PubMed  Google Scholar 

  4. Hitchen, P.G., Dell, A.: Bacterial glycoproteomics. Microbiology 152, 1575–1580 (2006)

    Article  CAS  PubMed  Google Scholar 

  5. Nothaft, H., Szymanski, C.M.: Protein glycosylation in bacteria: sweeter than ever. Nat. Rev. Microbiol. 8, 765–778 (2010)

    Article  CAS  PubMed  Google Scholar 

  6. Messner, P.: Bacterial glycoproteins. Glycoconj. J. 14, 3–11 (1997)

    Article  CAS  PubMed  Google Scholar 

  7. Messner, P., Sleytr, U.B.: Bacterial surface layer glycoproteins. Glycobiology 1, 545–551 (1991)

    Article  CAS  PubMed  Google Scholar 

  8. Ristl, R., Steiner, K., Zarschler, K., Zayni, S., Messner, P., Schäffer, C.: The S-Layer glycome—adding to the sugar coat of bacteria. Int. J. Microbiol. 2011, 127870 (2011)

    Article  PubMed Central  PubMed  Google Scholar 

  9. Messner, P., Steiner, K., Zarschler, K., Schäffer, C.: S-layer nanoglycobiology of bacteria. Carbohydr. Res. 343, 1934–1951 (2008)

    Article  CAS  PubMed  Google Scholar 

  10. Hartley, M.D., Morrison, M.J., Aas, F.E., Børud, B., Koomey, M., Imperiali, B.: Biochemical characterization of the O-linked glycosylation pathway in Neisseria gonorrhoeae responsible for biosynthesis of protein glycans containing N, N′-diacetylbacillosamine. Biochemistry 50, 4936–4948 (2011)

    Google Scholar 

  11. Logan, S.M.: Flagellar glycosylation—a new component of the motility repertoire? Microbiology 152, 1249–1262 (2006)

    Article  CAS  PubMed  Google Scholar 

  12. Dobos, K.M., Swiderek, K., Khoo, K.-H., Brennann, P.J., Belisle, J.T.: Evidence for glycosylation sites on the 45-kilodalton glycoprotein of Mycobacterium tuberculosis. Infect. Immun. 63, 2846–2853 (1995)

    CAS  PubMed Central  PubMed  Google Scholar 

  13. Karlyshev, A.V., Everest, P., Linton, D., Cawthraw, S., Newell, D.G., Wren, B.W.: The Campylobacter jejuni general glycosylation system is important for attachment to human epithelial cells and in the colonization of chicks. Microbiology 150, 1957–1964 (2004)

    Article  CAS  PubMed  Google Scholar 

  14. Szymanski, C.M., Wren, B.W.: Protein glycosylation in bacterial mucosal pathogens. Nat. Rev. Microbiol. 3, 225–237 (2005)

    Article  CAS  PubMed  Google Scholar 

  15. Szymanski, C.M., Yao, R., Ewing, C.P., Trust, T.J., Guerry, P.: Evidence for a system of general protein glycosylation in Campylobacter jejuni. Mol. Microbiol. 32, 1022–1030 (1999)

    Article  CAS  PubMed  Google Scholar 

  16. Wacker, M., Linton, D., Hitchen, P.G., Nita-Lazar, M., Haslam, S.M., North, J.S., Panico, M., Morris, H.R., Dell, A., Wren, B.W., Aebi, M.: N-linked glycosylation in Campylobacter jejuni and its functional transfer into E. coli. Science 298, 1790–1793 (2002)

    Google Scholar 

  17. Ku, S.C., Schulz, B.L., Power, P.M., Jennings, M.P.: The pilin O-glycosylation pathway of pathogenic Neisseria is a general system that glycosylates AniA, an outer membrane nitrite reductase. Biochem. Biophys. Res. Comm. 378, 84–89 (2009)

    Article  CAS  PubMed  Google Scholar 

  18. Fletcher, C.M., Coyne, M.J., Villa, O.F., Chatzidaki-Livanis, M., Comstock, L.E.: A general O-glycosylation system important to the physiology of a major human intestinal symbiont. Cell 137, 321–331 (2009)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  19. Posch, G., Pabst, M., Brecker, L., Altmann, F., Messner, P., Schäffer, C.: Characterization and scope of S-layer protein O-glycosylation in Tannerella forsythia. J. Biol. Chem. 286, 38714–38724 (2011)

    Article  CAS  PubMed  Google Scholar 

  20. Giraffa, G., Chanishvili, N., Widyastuti, Y.: Importance of lactobacilli in food and feed biotechnology. Res. Microbiol. 161, 480–487 (2010)

    Article  PubMed  Google Scholar 

  21. Helanto, M., Kiviharju, K., Leisola, M., Nyyssölä, A.: Metabolic engineering of Lactobacillus plantarum for production of L-ribulose. Appl. Environ. Microbiol. 73, 7083–7091 (2007)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  22. Peterbauer, C., Maischberger, T., Haltrich, D.: Food-grade gene expression in lactic acid bacteria. Biotechnol. J. 6, 1147–1161 (2011)

    Article  CAS  PubMed  Google Scholar 

  23. Konings, W.N., Kok, J., Kuipers, O.P., Poolman, B.: Lactic acid bacteria: the bugs of the new millennium. Curr. Opin. Microbiol. 3, 276–282 (2000)

    Article  CAS  PubMed  Google Scholar 

  24. Solá, R.J., Griebenow, K.: Glycosylation of therapeutic proteins. BioDrugs 24, 9–21 (2010)

    Article  PubMed Central  PubMed  Google Scholar 

  25. Wells, J.M.: Immunomodulatory mechanisms of lactobacilli. Microb. Cell Fact. 10, S17 (2011)

    Article  PubMed Central  PubMed  Google Scholar 

  26. Möschl, A., Schäffer, C., Sleytr, U.B., Messner, P., Christian, R., Schulz, G.: Characterization of the S-layer glycoproteins of two lactobacilli. In: Beveridge, T.J., Koval, S.F. (eds.) Advances in bacterial paracrystalline surface layers, vol. 252, pp. 281–284. Plenum Press, New York (1993)

    Chapter  Google Scholar 

  27. Mozes, N., Lortal, S.: X-ray photoelectron spectroscopy and biochemical analysis of the surface of Lactobacillus helveticus ATCC 12046. Microbiology 141, 11–19 (1995)

    Article  CAS  Google Scholar 

  28. Konstantinov, S.R., Smidt, H., de Vos, W.M., Bruijns, S.C.M., Singh, S.K., Valence, F., Molle, D., Lortal, S., Altermann, E., Klaenhammer, T.R., van Kooyk, Y.: S layer protein A of Lactobacillus acidophilus NCFM regulates immature dendritic cell and T cell functions. Proc. Natl. Acad. Sci. U. S. A. 105, 19474–19479 (2008)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  29. Mobili, P., los Ángeles Serradell, M., Trejo, S.A., Avilés Puigvert, F.X., Abraham, A.G., Antoni, G.L.: Heterogeneity of S-layer proteins from aggregating and non-aggregating Lactobacillus kefir strains. Antonie van Leeuwenhoek 95, 363–372 (2009)

  30. Messner, P., Schäffer, C., Egelseer, E., Sleytr, U.: Occurrence, structure, chemistry, genetics, morphogenesis, and functions of S-Layers. In: König, H., Claus, H., Varma, A. (eds.) Prokaryotic cell wall compounds—structure and biochemistry, pp. 53–109. Springer, Berlin (2010)

    Chapter  Google Scholar 

  31. Kawamura, T., Shockman, G.D.: Purification and some properties of the endogenous, autolytic N-acetylmuramoylhydrolase of Streptococcus faecium, a bacterial glycoenzyme. J. Biol. Chem. 258, 9514–9521 (1983)

    CAS  PubMed  Google Scholar 

  32. Fredriksen, L., Mathiesen, G., Moen, A., Bron, P.A., Kleerebezem, M., Eijsink, V.G.H., Egge-Jacobsen, W.: The major autolysin Acm2 from Lactobacillus plantarum undergoes cytoplasmic O-glycosylation. J. Bacteriol. 194, 325–333 (2011)

    Article  PubMed  Google Scholar 

  33. Rolain, T., Bernard, E., Beaussart, A., Degand, H., Courtin, P., Egge-Jacobsen, W., Bron, P.A., Morsomme, P., Kleerebezem, M., Chapot-Chartier, M.P., Dufrene, Y.F., Hols, P.: O-glycosylation as a novel control mechanism of peptidoglycan hydrolase activity. J. Biol. Chem. 288, 22233–22247 (2013)

    Article  CAS  PubMed  Google Scholar 

  34. Lebeer, S., Claes, I.J.J., Balog, C.I.A., Schoofs, G., Verhoeven, T.L.A., Nys, K., von Ossowski, I., de Vos, W.M., Tytgat, H.L.P., Agostinis, P., Palva, A., Van Damme, E.J.M., Deelder, A.M., de Keersmaecker, S.C.J., Wuhrer, M., Vanderleyden, J.: The major secreted protein Msp1/p75 is O-glycosylated in Lactobacillus rhamnosus GG. Microb. Cell Fact. 11, 15 (2012)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  35. Stepper, J., Shastri, S., Loo, T.S., Preston, J.C., Novak, P., Man, P., Moore, C.H., Havlíček, V., Patchett, M.L., Norris, G.E.: Cysteine S-glycosylation, a new post-translational modification found in glycopeptide bacteriocins. FEBS Lett. 585, 645–650 (2011)

    Article  CAS  PubMed  Google Scholar 

  36. Venugopal, H., Edwards, P.J.B., Schwalbe, M., Claridge, J.K., Libich, D.S., Stepper, J., Loo, T., Patchett, M.L., Norris, G.E., Pascal, S.M.: Structural, dynamic, and chemical characterization of a novel S-glycosylated bacteriocin. Biochemistry 50, 2748–2755 (2011)

    Article  CAS  PubMed  Google Scholar 

  37. Lebeer, S., Verhoeven, T.L.A., Francius, G., Schoofs, G., Lambrichts, I., Dufrene, Y., Vanderleyden, J., De Keersmaecker, S.C.J.: Identification of a gene cluster for the biosynthesis of a long, galactose-rich exopolysaccharide in Lactobacillus rhamnosus GG and functional analysis of the priming glycosyltransferase. Appl. Environ. Microbiol. 75, 3554–3563 (2009)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  38. Denou, E., Pridmore, R.D., Berger, B., Panoff, J.M., Arigoni, F., Brussow, H.: Identification of genes associated with the long-gut-persistence phenotype of the probiotic Lactobacillus johnsonii strain NCC533 using a combination of genomics and transcriptome analysis. J. Bacteriol. 190, 3161–3168 (2008)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  39. Marco, M.L., de Vries, M.C., Wels, M., Molenaar, D., Mangell, P., Ahrne, S., de Vos, W.M., Vaughan, E.E., Kleerebezem, M.: Convergence in probiotic Lactobacillus gut-adaptive responses in humans and mice. ISME J. 4, 1481–1484 (2010)

    Article  CAS  PubMed  Google Scholar 

  40. Heinl, S., Spath, K., Egger, E., Grabherr, R.: Sequence analysis and characterization of two cryptic plasmids derived from Lactobacillus buchneri CD034. Plasmid 66, 159–168 (2011)

    Article  CAS  PubMed  Google Scholar 

  41. Spath, K., Heinl, S., Egger, E., Grabherr, R.: Lactobacillus plantarum and Lactobacillus buchneri as expression systems: evaluation of different origins of replication for the design of suitable shuttle vectors. Mol. Biotechnol. 52, 40–48 (2012)

    Article  CAS  PubMed  Google Scholar 

  42. Liu, S., Skinner-Nemec, K.A., Leathers, T.D.: Lactobacillus buchneri strain NRRL B-30929 converts a concentrated mixture of xylose and glucose into ethanol and other products. J. Ind. Microbiol. Biotechnol. 35, 75–81 (2008)

    Article  CAS  PubMed  Google Scholar 

  43. Zeng, X.Q., Pan, D.D., Guo, Y.X.: The probiotic properties of Lactobacillus buchneri P2. J. Appl. Microbiol. 108, 2059–2066 (2010)

    CAS  PubMed  Google Scholar 

  44. Radovanovic, R.S., Katic, V.: Influence of lactic acid bacteria isolates on Staphylococcus aureus growth in skimmed milk. Bulg. J. Agric. Sci. 15, 196–203 (2009)

    Google Scholar 

  45. Kõll, P., Mändar, R., Smidt, I., Hütt, P., Truusalu, K., Mikelsaar, R.-H., Shchepetova, J., Krogh-Andersen, K., Marcotte, H., Hammarström, L., Mikelsaar, M.: Screening and evaluation of human intestinal lactobacilli for the development of novel gastrointestinal probiotics. Curr. Microbiol. 61, 560–566 (2010)

    Article  PubMed  Google Scholar 

  46. Danner, H., Holzer, M., Mayrhuber, E., Braun, R.: Acetic acid increases stability of silage under aerobic conditions. Appl. Environ. Microbiol. 69, 562–567 (2003)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  47. Driehuis, F., Oude Elferink, S.J.W.H., Spoelstra, S.F.: Anaerobic lactic acid degradation during ensilage of whole crop maize inoculated with Lactobacillus buchneri inhibits yeast growth and improves aerobic stability. J. Appl. Microbiol. 87, 583–594 (1999)

    Article  PubMed  Google Scholar 

  48. Holzer, M., Mayrhuber, E., Danner, H., Braun, R.: The role of Lactobacillus buchneri in forage preservation. Trends Biotechnol. 21, 282–287 (2003)

    Article  CAS  PubMed  Google Scholar 

  49. Kung, L.J., Taylor, C.C., Lynch, M.P., Neylon, J.M.: The effect of treating alfalfa with Lactobacillus buchneri 40788 on silage fermentation, aerobic stability, and nutritive value for lactating dairy cows. J. Dairy Sci. 86, 336–343 (2003)

    Article  CAS  PubMed  Google Scholar 

  50. Oude Elferink, S.J.W.H., Krooneman, J., Gottschal, J.C., Spoelstra, S.F., Faber, F., Driehuis, F.: Anaerobic conversion of lactic acid to acetic acid and 1,2-propanediol by Lactobacillus buchneri. Appl. Environ. Microbiol. 67, 125–132 (2001)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  51. Schmidt, R.J., Kung, L.J.: The effects of Lactobacillus buchneri with or without a homolactic bacterium on the fermentation and aerobic stability of corn silages made at different locations. J. Dairy Sci. 93, 1616–1624 (2010)

    Article  CAS  PubMed  Google Scholar 

  52. Heinl, S., Wibberg, D., Eikmeyer, F., Szczepanowski, R., Blom, J., Linke, B., Goesmann, A., Grabherr, R., Schwab, H., Pühler, A., Schlüter, A.: Insights into the completely annotated genome of Lactobacillus buchneri CD034, a strain isolated from stable grass silage. J. Biotechnol. 161, 153–166 (2012)

    Article  CAS  PubMed  Google Scholar 

  53. Liu, S., Leathers, T.D., Copeland, A., Chertkov, O., Goodwin, L., Mills, D.A.: Complete genome sequence of Lactobacillus buchneri NRRL B-30929, a novel strain from a commercial ethanol plant. J. Bacteriol. 193, 4019–4020 (2011)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  54. Liu, S., Bischoff, K.M., Hughes, S.R., Leathers, T.D., Price, N.P., Qureshi, N., Rich, J.O.: Conversion of biomass hydrolysates and other substrates to ethanol and other chemicals by Lactobacillus buchneri. Lett. Appl. Microbiol. 48, 337–342 (2009)

    Article  CAS  PubMed  Google Scholar 

  55. De Man, J.C., Rogosa, M., Sharpe, M.E.: A medium for the cultivation of lactobacilli. J. Appl. Microbiol. 23, 130–135 (1960)

    Google Scholar 

  56. Sleytr, U.B., Messner, P., Pum, D.: Analysis of crystalline bacterial surface layers by freeze-etching, metal shadowing, negative staining and ultrathin sectioning. Methods Microbiol. 20, 29–60 (1988)

    Article  Google Scholar 

  57. Sekot, G., Posch, G., Oh, Y., Zayni, S., Mayer, H., Pum, D., Messner, P., Hinterdorfer, P., Schäffer, C.: Analysis of the cell surface layer ultrastructure of the oral pathogen Tannerella forsythia. Arch. Microbiol. 196, 525–539 (2012)

    Article  Google Scholar 

  58. Laemmli, U.K.: Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685 (1970)

    Article  CAS  PubMed  Google Scholar 

  59. Hart, C., Schulenberg, B., Steinberg, T.H., Leung, W.-Y., Patton, W.F.: Detection of glycoproteins in polyacrylamide gels and on electroblots using Pro-Q Emerald 488 dye, a fluorescent periodate Schiff-base stain. Electrophoresis 24, 588–598 (2003)

    Article  CAS  PubMed  Google Scholar 

  60. Taylor, A.M., Holst, O., Thomas-Oates, J.: Mass spectrometric profiling of O-linked glycans released directly from glycoproteins in gels using in-gel reductive β-elimination. Proteomics 6, 2936–2946 (2006)

    Article  CAS  PubMed  Google Scholar 

  61. Packer, N.H., Lawson, M.A., Jardine, D.R., Redmond, J.W.: A general approach to desalting oligosaccharides released from glycoproteins. Glycoconj. J. 15, 737–747 (1998)

    Article  CAS  PubMed  Google Scholar 

  62. Pabst, M., Altmann, F.: Influence of electrosorption, solvent, temperature, and ion polarity on the performance of LC-ESI-MS using graphitic carbon for acidic oligosaccharides. Anal. Chem. 80, 7534–7542 (2008)

    Article  CAS  PubMed  Google Scholar 

  63. Stadlmann, J., Pabst, M., Kolarich, D., Kunert, R., Altmann, F.: Analysis of immunoglobulin glycosylation by LC-ESI-MS of glycopeptides and oligosaccharides. Proteomics 8, 2858–2871 (2008)

    Article  CAS  PubMed  Google Scholar 

  64. Lee, Y.: High-performance anion-exchange chromatography for carbohydrate analysis. Anal. Biochem. 189, 151–162 (1990)

    Article  CAS  PubMed  Google Scholar 

  65. Pabst, M., Bondili, J.S., Stadlmann, J., Mach, L., Altmann, F.: Mass + retention time = structure: a strategy for the analysis of N-glycans by carbon LC-ESI-MS and its application to fibrin N-glycans. Anal. Chem. 79, 5051–5057 (2007)

    Article  CAS  PubMed  Google Scholar 

  66. Hanisch, F.-G., Müller, S.: Approaches to the O-glycoproteome. In: The proteomics protocols handbook. pp. 439–457. Humana Press Inc., Totowa, New York (2005)

  67. Masuda, K., Kawata, T.: Characterization of a regular array in the wall of Lactobacillus buchneri and its reattachment to the other wall components. J. Gen. Microbiol. 124, 81–90 (1981)

    CAS  Google Scholar 

  68. Åvall-Jääskeläinen, S., Palva, A.: Lactobacillus surface layers and their applications. FEMS Microbiol. Rev. 29, 511–529 (2005)

    Article  PubMed  Google Scholar 

  69. van Roosmalen, M.L., Geukens, N., Jongbloed, J.D.H., Tjalsma, H., Dubois, J.-Y.F., Bron, S., van Dijl, J.M., Anné, J.: Type I signal peptidases of Gram-positive bacteria. Biochim. Biophys. Acta, Mol. Cell Res. 1694, 279–297 (2004)

    Article  PubMed  Google Scholar 

  70. Hynönen, U., Palva, A.: Lactobacillus surface layer proteins: structure, function and applications. Appl. Microbiol. Biotechnol. 97, 5225–5243 (2013)

    Article  PubMed Central  PubMed  Google Scholar 

  71. Kleerebezem, M., Hols, P., Bernard, E., Rolain, T., Zhou, M., Siezen, R.J., Bron, P.A.: The extracellular biology of the lactobacilli. FEMS Microbiol. Rev. 34, 199–230 (2010)

    Article  CAS  PubMed  Google Scholar 

  72. Steiner, K., Hanreich, A., Kainz, B., Hitchen, P.G., Dell, A., Messner, P., Schäffer, C.: Recombinant glycans on an S-layer self-assembly protein: a new dimension for nanopatterned biomaterials. Small 4, 1728–1740 (2008)

    Article  CAS  PubMed  Google Scholar 

  73. Zarschler, K., Janesch, B., Pabst, M., Altmann, F., Messner, P., Schäffer, C.: Protein tyrosine O-glycosylation—a rather unexplored prokaryotic glycosylation system. Glycobiology 20, 787–798 (2010)

    Google Scholar 

  74. Janesch, B., Messner, P., Schäffer, C.: Are the surface layer homology domains essential for cell surface display and glycosylation of the S-layer protein from Paenibacillus alvei CCM 2051T? J. Bacteriol. 195, 565–575 (2012)

    Google Scholar 

  75. Huard, C., Miranda, G., Wessner, F., Bolotin, A., Hansen, J., Foster, S.J., Chapot-Chartier, M.-P.: Characterization of AcmB, an N-acetylglucosaminidase autolysin from Lactococcus lactis. Microbiology 149, 695–705 (2003)

    Article  CAS  PubMed  Google Scholar 

  76. Claes, I.J.J., Schoofs, G., Regulski, K., Courtin, P., Chapot-Chartier, M.-P., Rolain, T., Hols, P., von Ossowski, I., Reunanen, J., De Vos, M.D., Palva, A., Vanderleyden, J., De Keersmaecker, S.C.J., Lebeer, S.: Genetic and biochemical characterization of the cell wall hydrolase activity of the major secreted protein of Lactobacillus rhamnosus GG. PLoS One 7, e31588 (2012)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  77. Faridmoayer, A., Fentabil, M.A., Mills, D.C., Klassen, J.S., Feldman, M.F.: Functional characterization of bacterial oligosaccharyltransferases involved in O-linked protein glycosylation. J. Bacteriol. 189, 8088–8098 (2007)

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  78. Hug, I., Feldman, M.F.: Analogies and homologies in lipopolysaccharide and glycoprotein biosynthesis in bacteria. Glycobiology 21, 138–151 (2010)

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Siqing Liu (U.S. Department of Agriculture, Agricultural Research Service, Renewable Product Technology Research Unit, University of Illinois, USA) for kindly providing L. buchneri NRRL B-30929, and Andrea Scheberl and Sonja Zayni for excellent technical assistance.

Financial support came from the Austrian Science Fund FWF, projects P21954-B20 (to C.S.) and P24305-B20 (to P.M.), the PhD programme “BioToP - Biomolecular Technology of Proteins” (Austrian Science Fund, FWF project W1224), the Hochschuljubiläumsstiftung der Stadt Wien, project H-2442/2012 (to J.A.), and the Christian Doppler Laboratory for Genetically Engineered Lactic Acid Bacteria (to R.G.).

Author information

Author notes

  1. Martin Pabst

    Present address: Department of Chemistry and Applied Biosciences, ETH Zurich, Zurich, Switzerland

  2. Gerhard Sekot

    Present address: Austrian Centre of Industrial Biotechnology, Muthgasse 18, 1190, Vienna, Austria

Authors and Affiliations

  1. Department of NanoBiotechnology, NanoGlycobiology unit, Universität für Bodenkultur Wien, Muthgasse 11, 1190, Vienna, Austria

    Julia Anzengruber, Gerhard Sekot, Paul Messner & Christina Schäffer

  2. Department of Chemistry, Universität für Bodenkultur Wien, Muthgasse 18, 1190, Vienna, Austria

    Martin Pabst, Laura Neumann & Friedrich Altmann

  3. Christian Doppler Laboratory for Genetically Engineered Lactic Acid Bacteria, Department of Biotechnology, Universität für Bodenkultur Wien, Muthgasse 11, 1190, Vienna, Austria

    Stefan Heinl & Reingard Grabherr

Authors
  1. Julia Anzengruber
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Martin Pabst
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Laura Neumann
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gerhard Sekot
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Stefan Heinl
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Reingard Grabherr
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Friedrich Altmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Paul Messner
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Christina Schäffer
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Christina Schäffer.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Anzengruber, J., Pabst, M., Neumann, L. et al. Protein O-glucosylation in Lactobacillus buchneri . Glycoconj J 31, 117–131 (2014). https://doi.org/10.1007/s10719-013-9505-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10719-013-9505-7

Keywords

Search

Navigation