Functional characterization of the initiation enzyme of S-layer glycoprotein glycan biosynthesis in Geobacillus stearothermophilus NRS 2004/3a

Journal of Bacteriology

Volumn 189, Issue 7, 2007, Pages 2590-2598

  Steiner, Kerstin ^a   Novotny, René ^a   Patel, Kinnari ^b   Vinogradov, Evgenij ^c   Whitfield, Chris ^d   Valvano, Miguel A ^b   Messner, Paul ^a   Schäffer, Christina ^a  

^a UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

^c NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^d UNIVERSITY OF GUELPH   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; GALACTOSE; GALACTOSE 1 PHOSPHATE URIDYLYLTRANSFERASE; GLYCAN; GLYCOPROTEIN; PHOSPHORYLPOLYPRENOL; RHAMNOSE; S LAYER GLYCOPROTEIN; TRANSFERASE; UNCLASSIFIED DRUG; URIDINE DIPHOSPHATE GALACTOSE:PHOSPHORYLPOLYPRENOLGALACTOSE 1 PHOSPHATE TRANSFERASE WSAP;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL STRAIN; CARBOXY TERMINAL SEQUENCE; ENZYME ACTIVITY; ESCHERICHIA COLI; GEOBACILLUS STEAROTHERMOPHILUS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; SALMONELLA ENTERICA;

AMINO ACID SEQUENCE; BACILLACEAE; BACTERIAL PROTEINS; CARBOHYDRATE SEQUENCE; CONSERVED SEQUENCE; GALACTOSYLTRANSFERASES; LIPOPOLYSACCHARIDES; MEMBRANE GLYCOPROTEINS; MOLECULAR SEQUENCE DATA; PLASMIDS; POLYSACCHARIDES; PROTEIN CONFORMATION; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID;

ESCHERICHIA COLI; GEOBACILLUS STEAROTHERMOPHILUS; SALMONELLA ENTERICA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM;

EID: 34147139297     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.01592-06     Document Type: Article

References (55)

1. Almirón-Roig, E., F. Mulholland, M. J. Gasson, and A. M. Griffin. 2000. The complete cps gene cluster from Streptococcus thermophilus NCFB 2393 involved in the biosynthesis of a new exopolysaccharide. Microbiology 146:2793-2802.
2. Arechaga, I., B. Miroux, S. Karrasch, R. Huijhregts, B. de Kruijff, M. J. Runswick, and J. E. Walker. 2000. Characterisation of new intracellular membranes in Escherichia coli accompanying large scale over-production of the b subunit of F(1)F(0) ATP synthase. FEBS Lett. 482:215-219.
3. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
4. Chakraborty, A. K., H. Friebolin, and S. Stirm. 1980. Primary structure of the Escherichia coli serotype K30 capsular polysaccharide. J. Bacteriol. 141:971-972.
5. Charbonnier, F., T. Köhler, J. C. Pechere, and A. Dueruix. 2001. Overexpression, refolding, and purification of the histidine-tagged outer membrane efflux protein OprM of Pseudomonas aeruginosa. Protein Expr. Purif. 23:121-127.
6. Clarke, B. R., L. Cuthbertson, and C. Whitfield. 2004. Nonreducing terminal modifications determine the chain length of polymannose O antigens of Escherichia coli and couple chain termination to polymer export via an ATP-binding cassette transporter. J. Biol. Chem. 279:35709-35718.
7. Dodgson, C., P. Amor, and C. Whitfield. 1996. Distribution of the rol gene encoding the regulator of lipopolysaccharide O-chain length in Escherichia coli and its influence on the expression of group I capsular K antigens. J. Bacteriol. 178:1895-1902.
8. Drummelsmith, J., and C. Whitfield. 1999. Gene products required for surface expression of the capsular form of the group I K antigen in Escherichia coli (O9a:K30). Mol. Microbiol. 31:1321-1332.
9. Eichler, J., and M. M. W. Adams. 2005. Posttranslational protein modification in archaea. Microbiol. Mol. Biol. Rev. 69:393-425.
10. Feldman, M. F., M. Wacker, M. Hernandez, P. G. Hitchen, C. L. Marolda, M. Kowarik, H. R. Morris, A. Dell, M. A. Valvano, and M. Aehi. 2005. Engineering N-linked protein glycosylation with diverse O antigen lipopolysaccharide structures in Escherichia coli. Proc. Natl. Acad. Sci. USA 102:3016-3021.
11. Folch, J., M. Lees, and G. H. Sloane-Stanley. 1957. A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 226:497-509.
12. Grahenhorst, E.. P. Schlenke. S. Pohl, M. Nimtz, and H. S. Conradt. 1999. Genetic engineering of recombinant glycoproteins and the glycosylation pathway in mammalian host cells. Glycoconj. J. 16:81-97.
13. Graninger, M., B. Kneidinger, K. Bruno, A. Scheberl, and P. Messner. 2002. Homologs of the Rm1 enzymes from Salmonella enterica are responsible for dTDP-β-L-rhamnose biosynthesis in the gram-positive thermophile Aneurinibacillus thermoaerophilus DSM 10155. Appl. Environ. Microbiol. 68:3708-3715.
14. Hartmann, E., P. Messner, G. Allmaier, and H. König. 1993. Proposed pathway for biosynthesis of the S-layer glycoprotein of Bacillus alvei. J. Bacteriol. 175:4515-4519.
15. Hitchcock, P. J.. and T. M. Brown. 1983. Morphological heterogeneity among Salmonella lipopolysaccharide chemotypes in silver-stained polyacrylamide gels. J. Bacteriol. 154:269-277.
16. Hitchen, P. G., and A. Dell. 2006. Bacterial glycoproteomics. Microbiology 152:1575-1580.
17. Kneidinger, B., C. Marolda, M. Graninger, A. Zamyatina, F. McArthur, P. Kosma, M. A. Valvano, and P. Messner. 2002. Biosynthesis pathway of ADP-L-glycero-β-D-manno-heptose in Escherichia coli. J. Bacteriol. 184:363-369.
18. Kolkman, M. A., D. A. Morrison, B. A. van der Zeijst, and P. J. Nuijten. 1996. The capsule polysaccharide synthesis locus of Streptococcus pneumoniae serotype 14: identification of the glycosyl transferase gene cps14E. J. Bacteriol. 178:3736-3741.
19. Kolkman, M. A., B. A. van der Zeijst, and P. J., Nuijten, 1997. Functional analysis of glycosyltransferases encoded by the capsular polysaccharide biosynthesis locus of Streptococcus pneumoniae serotype 14. J. Biol. Chem. 272:19502-19508.
20. Laeminli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
21. Messner, P., F. Hollaus, and U. B. Sleytr. 1984. Paracrystalline cell wall surface layers of different Bacillus stearothermophilus strains. Int. J. Syst. Bacteriol. 34:202-210.
22. Messner, P., and C. Schäffer. 2003. Prokaryotic glycoproteins. Fortschr. Chem. Org. Naturst. 85:51-124.
23. Miroux, B., and J. E. Walker. 1996. Over-production of proteins in Escherichia coli: mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels. J. Mol. Biol. 260:289-298.
24. Novotny, R., A. Pföstl, P. Messner, and C. Schäffen 2004. Genetic organization of chromosomal S-layer glycan biosynthesis loci of Bacillaceae. Glycoconj. J. 20:435-447.
25. Novotny, R., C. Schäffer, J. Strauss, and P. Messner. 2004. S-layer glycan-specific loci on the chromosome of Geobacillus stearothermophilus NRS 2004/3a and dTDP-L-rhamnose biosynthesis potential of G. stearothermophilus strains. Microbiology 150:953-965.
26. Osborn, J. N., M. A. Cynkin, J. M. Gilhert, L. Müller, and M. Singh. 1972. Synthesis of bacterial O-antigens. Methods Enzymol. 28:583-601.
27. Pelosi, L., M. Boumedienne, N. Saksouk, J. Geiselmann, and R. A. Geremia. 2005. The glucosyl-l-phosphaie transferase WehA (Cap8E) primes the capsular polysaccharide repeat unit biosynthesis of Streptococcus pneumoniae serotype 8. Biochem. Biophys. Res. Commun. 327:857-865.
28. T J. Biol. Chem. 278:26410-26417.
29. Raetz, C. R. H., and C. Whitfield. 2002. Lipopolysaccharide endotoxins. Annu. Rev. Biochem. 71:635-700.
30. Rahn, A., and C. Whitfield. 2003. Transcriptional organization and regulation of the Escherichia coli K30 group 1 capsule biosynthesis (cps) gene cluster. Mol. Microbiol. 47:1045-1060.
31. Reeves, P. R., M. Hobbs, M. A. Valvano, M. Skurnik, C. Whitfield, D. Coplin, N. Kido, J. Klena, D. Maskell, C. R. H. Raetz, and P. D. Rick. 1996. Bacterial polysaccharide synthesis and gene nomenclature. Trends Microbiol. 4:495-503.
32. Rudd, P. M., T. Elliott, P. Cresswell, I. A. Wilson, and R. A. Dwek. 2001. Glycosylation and the immune system. Science 291:2370-2376.
33. Saidijam, M., G. Psakis, J. L. Clough, J. Meuller, S. Suzuki, C. J. Hoyle, S. L. Palmer, S. M. Morrison, M. K. Pos, R. C. Essenberg, M. C. Maiden, A. Abu-Bakr, S. G. Baumberg, A. A. Neyfakh, J. K. Griffith, M. J. Stark, A. Ward, J. O'Reilly, N. G. Rutherford, M. K. Phillips-Jones, and P. J. Henderson. 2003. Collection and characterisation of bacterial membrane proteins. FEBS Lett. 555:170-175.
34. Saldías, M. S. 2004. Functional analysis of WbaP, essential enzyme in the biosynthesis of O-antigen in Salmonella enterica. Ph.D. thesis. Universidad de Chile, Santiago, Chile.
35. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press. Cold Spring Harbor, NY.
36. Samuel, G., and P. Reeves. 2003. Biosynthesis of O-antigens: genes and pathways involved in nucleotide sugar precursor synthesis and O-antigen assembly. Carbohydr. Res. 338:2503-2519.
37. Saxon, E., and C. R. Bertozzi. 2001. Chemical and biological strategies for engineering cell surface glycosylation. Annu. Rev. Cell Dev. Biol. 17:1-23.
38. Schäffer. C., T. Wugeditsch, C. Neuninger, and P. Messner. 1996. Arc S-layer glycoproteins and lipopolysaccharides related? Microb. Drug Resist. 2:17-23.
39. Schäffer, C., T. Wugeditsch, H. Kählig, A. Scheherl, S. Zayni, and P. Messner. 2002. The surface layer (S-layer) glycoprotein of Geobacillus stearothermophilus NRS 2004/3a. Analysis of its glycosylation. J. Biol. Chem. 277:6230-6239.
40. Schaffer, C., T. Wugeditsch, P. Messner, and C. Whitfield. 2002. Functional expression of enterobacterial O-polysaccharide biosynthesis enzymes in Bacillus subtilis. Appl. Environ. Microbiol. 68:4722-4730.
41. Schäffer, C., and P. Messner. 2004. Surface-layer glycoproteins: an example for the diversity of bacterial glycosylalion with promising impacts on nano-biotechnology. Glycobiology 14:31R-42R.
42. Sleytr, U. B., M. Sára, D. Pum, B. Schuster, P. Messner, and C. Schäffer. 2002. Self-assembly protein systems: microbial S-layers, p. 285-338. In A. Steinbüchel and S. R. Fahnestock (ed.), Biopolymers, vol. 7. Polyamides and complex proteinaceous matrices. Wiley-VCH, Weinheim, Germany.
43. Steiner, K., G. Pohlentz, K. Dreisewerd, S. Berkenkamp, P. Messner, J. Peter-Katalinic, and C. Schäffer. 2006. New insights into the glycosylation of the surface layer protein SgsE from Geobacillus stearothermophilus NRS 2004/3a. J. Bacteriol. 188:7914-7921.
44. Stingele, F., J. W. Newell, and J. R. Neeser. 1999. Unraveling the function of glycosyltransferases in Streptococcus thermophilus Sfi6. J. Bacteriol. 181:6354-6360.
45. Szymanski, C. M., and B. W. Wren. 2005. Protein glycosylation in bacterial mucosal pathogens. Nat. Rev. Microbiol. 3:225-237.
46. Towbin, H., T. Staehelin, and J. Gordon. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76:4350-4354.
47. Tsai, C. M., and C. E. Frasch. 1982. A sensitive silver stain for detecting lipopolysaccharides in polyacrylamide gels. Anal. Biochem. 119:115-119.
48. Upreti, R. K., M. Kumar, and V. Shankar. 2003. Bacterial glycoproteins: functions, biosynthesis and applications. Proteomics 3:363-379.
49. Valvano, M. A. 2003. Export of O-specific lipopolysaccharide. Front. Biosci. 8:S452-S471.
50. Varki, A., R. Cummings, J. Esko, H. Freeze, G. Hart, and J. Marth (ed.). 1999. Essentials of glycobiology. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
51. Wacker, M., D. Linton, P. G. Hitchen, M. Nita-Lazar, S. M. Haslam, S. J. North, M. Panico, H. R. Morris, A. Dell, B. W. Wren, and M. Aebi. 2002. N-linked glycosylation in Campylobacter jejuni and its functional transfer into E. coli. Science 298:1790-1793.
52. Wang, L., and P. R. Reeves. 1994. Involvement of the galactosyl-1-phosphate transferase encoded by the Salmonella enterica rfbP gene in O-antigen sub-unit processing. J. Bacteriol. 176:4348-4356.
53. Wang, L., D. Liu, and P. R. Reeves. 1996. C-terminal half of Salmonella enterica WbaP (RfbP) is the galactosyl-1-phosphate transferase domain catalyzing the first step of O-antigen synthesis. J. Bacteriol. 178:2598-2604.
54. Westermeier, R. 1990. Electrophoresis-Praktikum, p. 189-196. VCH Verlagsgesellschaft, Weinhcim, Germany.
55. Whitfield, C. 2006. Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annu. Rev. Biochem. 75:39-68.