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Genetic organization of chromosomal S-layer glycan biosynthesis loci of Bacillaceae

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Abstract

S-layer glycoproteins are cell surface glycoconjugates that have been identified in archaea and in bacteria. Usually, S-layer glycoproteins assemble into regular, crystalline arrays covering the entire bacterium. Our research focuses on thermophilic Bacillaceae, which are considered a suitable model system for studying bacterial glycosylation. During the past decade, investigations of S-layer glycoproteins dealt with the elucidation of the highly variable glycan structures by a combination of chemical degradation methods and nuclear magnetic resonance spectroscopy. It was only recently that the molecular characterization of the genes governing the formation of the S-layer glycoprotein glycan chains has been initiated. The S-layer glycosylation (slg) gene clusters of four of the 11 known S-layer glycan structures from members of the Bacillaceae have now been studied. The clusters are ∼16 to ∼25 kb in size and transcribed as polycistronic units. They include nucleotide sugar pathway genes that are arranged as operons, sugar transferase genes, glycan processing genes, and transporter genes. So far, the biochemical functions only of the genes required for nucleotide sugar biosynthesis have been demonstrated experimentally. The presence of insertion sequences and the decrease of the G+C content at the slg locus suggest that the investigated organisms have acquired their specific S-layer glycosylation potential by lateral gene transfer. In addition, S-layer protein glycosylation requires the participation of housekeeping genes that map outside the cluster. The gene encoding the respective S-layer target protein is transcribed monocistronically and independently of the slg cluster genes. Its chromosomal location is not necessarily in close vicinity to the slg gene cluster. Published in 2004.

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References

  1. Benz I, Schmidt MA, Never say never again: Protein glycosylation in pathogenic bacteria, Mol Microbiol 45, 267–76 (2002).

    Article  PubMed  CAS  Google Scholar 

  2. Messner P, Schäffer C, Prokaryotic glycoproteins. In Progress in the Chemistry of Organic Natural Products, edited by Herz W, Falk H, Kirby GW(Springer-Verlag, Wien, 2003), vol. 85, pp. 51–124.

    Google Scholar 

  3. Moens S, Non-S-Layer glycoproteins: A review. In Glycomicrobiology, edited by Doyle RJ (Kluwer Academic/Plenum Publishers, New York, 2000), pp. 93–125.

    Google Scholar 

  4. Szymanski CM, Logan SM, Linton D, Wren BW, Campylobacter-a tale of two protein glycosylation systems, Trends Microbiol 11, 233–8 (2003).

    PubMed  CAS  Google Scholar 

  5. Upreti RK, Kumar M, Shankar V, Bacterial glycoproteins: Functions, biosynthesis and applications, Proteomics 3, 363–79 (2003).

    Article  PubMed  CAS  Google Scholar 

  6. Castric P, Cassels FJ, Carlson RW, Structural characterization of the Pseudomonas aeruginosa1244 pilin glycan, J Biol Chem 276, 26479–85 (2001), Correction, J Biol Chem 276, 36058 (2001).

    Article  PubMed  CAS  Google Scholar 

  7. Power PM, Jennings MP, The genetics of glycosylation in Gramnegative bacteria, FEMS Microbiol Lett 218, 211–22 (2003).

    Article  PubMed  CAS  Google Scholar 

  8. Thomas NA, Bardy SL, Jarrell KF, The archaeal flagellum: A different kind of prokaryotic motility structure, FEMS Microbiol Rev 25, 147–74 (2001).

    Article  PubMed  CAS  Google Scholar 

  9. Sleytr UB, Messner P, Crystalline bacterial cell surface layers (S-layers). In Desk Encyclopedia of Microbiology, edited by Schaechter M(Elsevier Science USA, San Diego, 2003), pp. 286–93.

    Google Scholar 

  10. Sleytr UB, Sára M, Pum D, Schuster B, Messner P, Schäffer C, Self-assembly protein systems: Microbial S-layers. In Biopolymers, Polyamides and Complex Proteinaceous Matrices I, edited by Steinbüchel A, Fahnestock SR (Wiley-VCH, Weinheim, 2002), vol. 7, pp. 285–338.

    Google Scholar 

  11. Schäffer C, Wugeditsch T, Kählig H, Scheberl A, Zayni S, Messner P, The surface layer (S-layer) glycoprotein of Geobacillus stearothermophilusNRS 2004/3a. Analysis of its glycosylation, J Biol Chem 277, 6230–9 (2002).

    Article  PubMed  CAS  Google Scholar 

  12. Wugeditsch T, Zachara NE, Puchberger M, Kosma P, Gooley AA, Messner P, Structural heterogeneity in the core oligosaccharide of the S-layer glycoprotein from Aneurinibacillus thermoaerophilusDSM 10155, Glycobiology 8,787–95 (1999).

    Article  Google Scholar 

  13. Sumper M, Wieland FT, Bacterial glycoproteins. In Glycoproteins, edited by Montreuil J, Vliegenthart JFG, Schachter H (Elsevier, Amsterdam, 1995), pp. 455–73.

    Google Scholar 

  14. Meier-Stauffer K, Busse HJ, Rainey FA, Burghardt J, Scheberl A, Hollaus F, Kuen B, Makristathis A, Sleytr UB, Messner P, Description of Bacillus thermoaerophilussp. nov., to include sugar beet isolates and Bacillus brevisATCC 12990, Int J Syst Bacteriol 46, 532–41 (1996).

    Article  CAS  Google Scholar 

  15. Wugeditsch T, Strukturanalyse des S-Schichtglykoproteins und Zellwand-Aminozuckerpolymers von Aneurinibacillus thermoaerophilus DSM 10155(Doctoral thesis, Universität für Bodenkultur Wien, 1998), 238 pages.

  16. Schäffer C, Messner P, Surface-layer glycoproteins: An example for the diversity of bacterial glycosylation with promising impacts on nanobiotechnology, Glycobiology 14, 31R–42R (2004).

    Article  PubMed  CAS  Google Scholar 

  17. Novotny R, Schäffer C, Strauss J, Messner P, S-layer glycanspecific loci on the chromosome of Geobacillus stearothermophilusNRS 2004/3a and dTDP-L-rhamnose biosynthesis potential of Geobacillus stearothermophilusstrains, Microbiology 150, 953–65 (2004).

    Article  PubMed  CAS  Google Scholar 

  18. Christian R, Schulz G, Unger FM, Messner P, Küpcü Z, Sleytr UB, Structure of a rhamnan from the surface-layer glycoprotein of Bacillus stearothermophilusstrain NRS 2004/3a, Carbohydr Res 150, 265–72 (1986). 447

    Article  PubMed  CAS  Google Scholar 

  19. Kosma P, Wugeditsch T, Christian R, Zayni S, Messner P, Glycan structure of a heptose-containing S-layer glycoprotein of Bacillus thermoaerophilus, Glycobiology 5, 791–6 (1995). Erratum in: Glycobiology vn6, 5 (1996).

    PubMed  CAS  Google Scholar 

  20. Kosma P, Neuninger C, Christian R, Schulz G, Messner P, Glycan structure of the S-layer glycoprotein of Bacillussp. L420-91, Glycoconj J 1, 99–107 (1995).

    Article  Google Scholar 

  21. Schäffer C, Müller N, Christian R, Graninger M, Wugeditsch T, Scheberl A, Messner P, Complete glycan structure of the Slayer glycoprotein of Aneurinibacillus thermoaerophilusGS4-97, Glycobiology 4, 407–14 (1999).

    Article  Google Scholar 

  22. Altman E, Schäffer C, Brisson JR, Messner P, Characterization of the glycan structure of a major glycopeptide from the surface layer glycoprotein of Clostridium thermosaccharolyticumE207-71, Eur J Biochem 229, 308–15 (1995).

    Article  PubMed  CAS  Google Scholar 

  23. Markovitz A, Biosynthesis of guanosine diphosphate D-rhamnose and guanosine diphosphate D-talomethylose from guanosine diphosphate α-mannose, J Biol Chem 239, 2091–8 (1964).

    PubMed  CAS  Google Scholar 

  24. Giraud M-F, Naismith JH, The rhamnose pathway, Curr Opin Struct Biol 10, 687–96 (2000).

    Google Scholar 

  25. Kneidinger B, Graninger M, Adam G, Puchberger M, Kosma P, Zayni S, Messner P, Identification of two GDP-6-deoxy-D-lyxo-4-hexulose reductases synthesizing GDP-D-rhamnose in Aneurinibacillus thermoaerophilusL420-91T, J Biol Chem 276, 5577–83 (2001).

    Article  PubMed  CAS  Google Scholar 

  26. Kneidinger B, Graninger M, Messner P, Chromosome walking by cloning of distinct PCR fragments, Biotechniques 30, 248–9 (2001).

    PubMed  CAS  Google Scholar 

  27. Jiang S-M, Wang L, Reeves PR, Molecular characterization of Streptococcus pneumoniaetype 4, 6B, 8, and 18C capsular polysaccharide gene clusters, Infect Immun 69, 1244–55 (2001).

    Article  PubMed  CAS  Google Scholar 

  28. Tsukioka Y, Yamashita Y, Oho T, Nakano Y, Koga T, Biological function of the dTDP-rhamnose synthesis pathway in Streptococcus mutans, J Bacteriol 179, 1126–34 (1997).

    PubMed  CAS  Google Scholar 

  29. Mitchison M, Bulach DM, Vinh T, Rajakumar K, Faine S, Adler B, Identification and characterization of the dTDP-rhamnose biosynthesis and transfer genes of the lipopolysaccharide-related rfblocus in Leptospira interrogansserovar Copenhageni, J Bacteriol 179, 1262–7 (1997).

    PubMed  CAS  Google Scholar 

  30. Nakano Y, Yoshida Y, Suzuki N, Yamashita Y, Koga T,Agene cluster for the synthesis of serotype d-specific polysaccharide antigen in Actinobacillus actinomycetemcomitans, Biochim Biophys Acta 1493, 259–63 (2000).

    PubMed  CAS  Google Scholar 

  31. Wang L, Liu D, Reeves PR, C-terminal half of Salmonella entericaWbaP (RfbP) is the galactosyl-1-phosphate transferase domain catalyzing the first step of O-antigen synthesis, J Bacteriol 178,2598–604 (1996).

    PubMed  CAS  Google Scholar 

  32. Pfoestl A, Hofinger A, Kosma P, Messner P, Biosynthesis of dTDP-3-acetamido-3,6-dideoxy-α-D-galactose in Aneurinibacillus thermoaerophilusL420-91T, J Biol Chem 278, 26410–7 (2003).

    Article  PubMed  CAS  Google Scholar 

  33. Bengoechea JA, Pinta E, Salminen T, Oertelt C, Holst O, Radziejewska-Lebrecht J, Piotrowska-Seget Z, Venho R, Skurnik M, Functional characterization of Gne (UDP-Nacetylglucosamine-4-epimerase), Wzz (chain length determinant), and Wzy (O-antigen polymerase) of Yersinia enterocoliticaserotype O:8, J Bacteriol 184, 4277–87 (2002).

    Article  PubMed  CAS  Google Scholar 

  34. Estrela AI, Pooley HM, de Lencastre H, Karamata D, Genetic and biochemical characterization of Bacillus subtilis168 mutants specifically blocked in the synthesis of the teichoic acid poly(3-O-β-D-glucopyranosyl-N-acetylgalactosamine 1-phosphate): gneA, a new locus, is associated with UDP-N-acetylglucosamine 4-epimerase activity, J Gen Microbiol 137, 943–50 (1991).

    PubMed  CAS  Google Scholar 

  35. Reeves PR, Wang L, Genomic organization of LPS-specific loci, Curr Top Microbiol Immunol 264, 109–35 (2002).

    Google Scholar 

  36. Jolly L, Stingele F, Molecular organization and functionality of exopolysaccharide gene clusters in lactic acid bacteria, Int Dairy J 11, 733–45 (2001).

    Article  CAS  Google Scholar 

  37. Skurnik M, Molecular genetics, biochemistry and biological role of Yersinialipopolysaccharide, Adv Exp Med Biol 529,187–97 (2003).

    Article  Google Scholar 

  38. Hobbs M, Reeves PR, The JUMPstart sequence: A 39 bp element common to several polysaccharide gene clusters, Mol Microbiol 12, 855–56 (1994).

    PubMed  CAS  Google Scholar 

  39. Keenleyside WJ, Whitfield C, Genetics and biosynthesis of lipopolysaccharide O-antigens. In Endotoxin in Health and Disease, edited by Brade H, Opal SM, Vogel SN, Morrison DC (Marcel Dekker, New York, Basel, 1999), pp. 331–58.

    Google Scholar 

  40. Graninger M, Kneidinger B, Bruno K, Scheberl A, Messner P, Homologs of the Rml enzymes from Salmonella entericaare responsible for dTDP-β-L-rhamnose biosynthesis in the gram-positive thermophile Aneurinibacillus thermoaerophilusDSM 10155, Appl Environ Microbiol 68, 3708–15 (2002).

    Article  PubMed  CAS  Google Scholar 

  41. Kneidinger B, Graninger M, Puchberger M, Kosma P, Messner P, Biosynthesis of nucleotide-activated D-glycero-D-mannoheptose, J Biol Chem 276, 20935–44 (2001).

    Article  PubMed  CAS  Google Scholar 

  42. Kneidinger B, Marolda C, Graninger M, Zamyatina A, McArthur F, Kosma P, Valvano MA, Messner P, Biosynthesis pathway of ADP-L-glycero-β-D-manno-heptose in Escherichia coli, J Bacteriol 184, 363–69 (2002).

    Article  PubMed  CAS  Google Scholar 

  43. Ma Y, Stern RJ, Scherman MS, Vissa VD, Yan W, Jones VC, Zhang F, Franzblau SG, Lewis WH, McNeil MR, Drug targeting Mycobacterium tuberculosiscell wall synthesis: Genetics of dTDP-rhamnose synthetic enzymes and development of a microtiter plate-based screen for inhibitors of conversion of dTDPglucose to dTDP-rhamnose, Antimicrob Agents Chemother 45,1407–16 (2001).

    Article  PubMed  CAS  Google Scholar 

  44. Samuel G, Reeves P, Biosynthesis of O-antigens: Genes and pathways involved in nucleotide sugar precursor synthesis and Oantigen assembly, Carbohydr Res 338, 2503–19 (2003).

    Article  PubMed  CAS  Google Scholar 

  45. Whitfield C, Paiment A, Biosynthesis and assembly of Group 1 capsular polysaccharides in Escherichia coliand related extracellular polysaccharides in other bacteria, Carbohydr Res 338, 2491–502 (2003).

    Article  PubMed  CAS  Google Scholar 

  46. Whitfield C, Roberts IS, Structure, assembly and regulation of expression of capsules in Escherichia coli, Mol Microbiol 31, 1307–19 (1999).

    Article  PubMed  CAS  Google Scholar 

  47. Raetz CRH, Whitfield C, Lipopolysaccharide endotoxins, Annu Rev Biochem 71, 635–700 (2002).

    Google Scholar 

  48. Whitfield C, Biosynthesis of lipopolysaccharide O-antigens, Trends Microbiol 3, 178–85 (1995).

    Google Scholar 

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Correspondence to Christina Schäffer.

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Novotny, R., Pfoestl, A., Messner, P. et al. Genetic organization of chromosomal S-layer glycan biosynthesis loci of Bacillaceae . Glycoconj J 20, 435–447 (2003). https://doi.org/10.1023/B:GLYC.0000038290.74944.65

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