The amazing repertoire of glycoconjugates present on bacterial cell surfaces includes lipopolysaccharides, capsular polysaccharides, lipooligosaccharides, exopolysaccharides, and glycoproteins. While the former are constituents of Gram-negative cells, we review here the cell surface S-layer glycoproteins of Gram-positive bacteria. S-layer glycoproteins have the unique feature of self-assembling into 2D lattices providing a display matrix for glycans with periodicity at the nanometer scale. Typically, bacterial S-layer glycans are O-glycosidically linked to serine, threonine, or tyrosine residues, and they rely on a much wider variety of constituents, glycosidic linkage types, and structures than their eukaryotic counterparts. As the S-layer glycome of several bacteria is unravelling, a picture of how S-layer glycoproteins are biosynthesized is evolving. X-ray crystallography experiments allowed first insights into the catalysis mechanism of selected enzymes. In the future, it will be exciting to fully exploit the S-layer glycome for glycoengineering purposes and to link it to the bacterial interactome. 1. Introduction 1.1. The Sweet Cell Surface of Bacteria at a Glance Nature has equipped prokaryotic organisms from almost all phylogenetic branches with an amazing repertoire of components from its glycodiversification tool box, adding to the “sweetness” of their cell surface. The “sweetness” is derived from different kinds of polysaccharides, such as capsules or exopolysaccharides as well as glycoconjugates, such as lipopolysaccharides, lipooligosaccharides, and glycoproteins, all of which may additionally carry noncarbohydrate modifications. The complex type of biosynthesis of these prokaryotic carbohydrate components is truly amazing, and despite the tremendous progress in molecular biology it is still very difficult to see at present how the sequence of enzymatic reactions involved in the controlled biosynthesis of carbohydrate chains is regulated. Thus, it is reasonable to believe that the cellular sugar coat serves an important biological function. Prokaryotic glycoconjugates derive most of their structural diversity from the identities of their unusual sugar moieties. The addition of sugars to a nonglycosylated biomolecule changes its size and shape and this is likely to affect the access of proteolytic enzymes. Further, it will influence factors such as solubility, heat stability as well as many physical and chemical properties. Based on these properties, cell surface glycosylation may protect the prokaryotic cell from desiccation and other
References
[1]
C. Whitfield, “Biosynthesis and assembly of capsular polysaccharides in Escherichia coli,” Annual Review of Biochemistry, vol. 75, pp. 39–68, 2006.
[2]
M. Abu-Qarn, J. Eichler, and N. Sharon, “Not just for Eukarya anymore: protein glycosylation in Bacteria and Archaea,” Current Opinion in Structural Biology, vol. 18, no. 5, pp. 544–550, 2008.
[3]
P. Messner, K. Steiner, K. Zarschler, and C. Sch？ffer, “S-layer nanoglycobiology of bacteria,” Carbohydrate Research, vol. 343, no. 12, pp. 1934–1951, 2008.
[4]
C. J. Thibodeaux, C. E. Melan？on III, and H.-W. Liu, “Natural-product sugar biosynthesis and enzymatic glycodiversification,” Angewandte Chemie—International Edition, vol. 47, no. 51, pp. 9814–9859, 2008.
[5]
M. F. Mescher and J. L. Strominger, “Purification and characterization of a prokaryotic glycoprotein from the cell envelope of Halobacterium salinarium,” The Journal of Biological Chemistry, vol. 251, no. 7, pp. 2005–2014, 1976.
[6]
U. B. Sleytr and K. J. I. Thorne, “Chemical characterization of the regularly arranged surface layers of Clostridium thermosaccharolyticum and Clostridium thermohydrosulfuricum,” Journal of Bacteriology, vol. 126, no. 1, pp. 377–383, 1976.
[7]
U. B. Sleytr, E. M. Egelseer, N. Ilk, D. Pum, and B. Schuster, “S-Layers as a basic building block in a molecular construction kit,” FEBS Journal, vol. 274, no. 2, pp. 323–334, 2007.
[8]
U. B. Sleytr and T. J. Beveridge, “Bacterial S-layers,” Trends in Microbiology, vol. 7, no. 6, pp. 253–260, 1999.
[9]
H. Claus, E. Aka, T. Debaerdemaeker, C. Evrard, J.-P. Declercq, and H. K？nig, “Primary structure of selected archaeal mesophilic and extremely thermophilic outer surface layer proteins,” Systematic and Applied Microbiology, vol. 25, no. 1, pp. 3–12, 2002.
[10]
C. Sch？ffer and P. Messner, “Surface-layer glycoproteins: an example for the diversity of bacterial glycosylation with promising impacts on nanobiotechnology,” Glycobiology, vol. 14, no. 8, pp. 31R–42R, 2004.
[11]
J. Eichler and M. W. W. Adams, “Posttranslational protein modification in Archaea,” Microbiology and Molecular Biology Reviews, vol. 69, no. 3, pp. 393–425, 2005.
[12]
M. Sumper and F. T. Wieland, “Bacterial glycoproteins,” in Glycoproteins, J. Montreuil, J. F. G. Vliegenthart, and H. Schachter, Eds., pp. 455–473, Elsevier, Amsterdam, The Netherlands, 1995.
[13]
U. B. Sleytr, P. Messner, D. Pum, and M. Sára, “Crystalline bacterial cell surface layers (S layers): from supramolecular cell structure to biomimetics and nanotechnology,” Angewandte Chemie—International Edition, vol. 38, no. 8, pp. 1034–1054, 1999.
[14]
M. Sára, “Conserved anchoring mechanisms between crystalline cell surface S-layer proteins and secondary cell wall polymers in Gram-positive bacteria?” Trends in Microbiology, vol. 9, no. 2, pp. 47–49, 2001.
[15]
C. Sch？ffer and P. Messner, “The structure of secondary cell wall polymers: how Gram-positive bacteria stick their cell walls together,” Microbiology, vol. 151, no. 3, pp. 643–651, 2005.
[16]
P. Messner and U. B. Sleytr, “Crystalline bacterial cell-surface layers,” Advances in Microbial Physiology, vol. 33, pp. 213–275, 1992.
[17]
M. Sára and U. B. Sleytr, “S-layer proteins,” Journal of Bacteriology, vol. 182, no. 4, pp. 859–868, 2000.
[18]
R. Novotny, A. Pfoestl, P. Messner, and C. Sch？ffer, “Genetic organization of chromosomal S-layer glycan biosynthesis loci of Bacillaceae,” Glycoconjugate Journal, vol. 20, no. 7-8, pp. 435–447, 2004.
[19]
S.-W. Lee, M. Sabet, H.-S. Um, J. Yang, H. C. Kim, and W. Zhu, “Identification and characterization of the genes encoding a unique surface (S-) layer of Tannerella forsythia,” Gene, vol. 371, no. 1, pp. 102–111, 2006.
[20]
C. M. Fletcher, M. J. Coyne, D. L. Bentley, O. F. Villa, and L. E. Comstock, “Phase-variable expression of a family of glycoproteins imparts a dynamic surface to a symbiont in its human intestinal ecosystem,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 7, pp. 2413–2418, 2007.
[21]
P. Kosma, C. Neuninger, R. Christian, G. Schulz, and P. Messner, “Glycan structure of the S-layer glycoprotein of Bacillus sp. L420-91,” Glycoconjugate Journal, vol. 12, no. 1, pp. 99–107, 1995.
[22]
P. Kosma, T. Wugeditsch, R. Christian, S. Zayni, and P. Messner, “Glycan structure of a heptose-containing S-layer glycoprotein of Bacillus thermoaerophilus,” Glycobiology, vol. 5, no. 8, pp. 791–796, 1995.
[23]
K. Meier-Stauffer, H.-J. Busse, and H.-J. Busse, “Description of Bacillus thermoaerophilus sp. nov., to include sugar beet isolates and Bacillus brevis ATCC 12990,” International Journal of Systematic Bacteriology, vol. 46, no. 2, pp. 532–541, 1996.
[24]
P. Messner, A. Scheberl, W. Schweigkofler, F. Hollaus, F. A. Rainey, J. Burghardt, and H. Prillinger, “Taxonomic comparison of different thermophilic sugar beet isolates with glycosylated surface layer (S-Layer) proteins and their affiliation to Bacillus smithii,” Systematic and Applied Microbiology, vol. 20, no. 4, pp. 559–565, 1997.
[25]
M. S. Sidhu and I. Olsen, “S-layers of Bacillus species,” Microbiology, vol. 143, no. 4, pp. 1039–1052, 1997.
[26]
Z. Xu, B. Yao, M. Sun, and Z. Yu, “Protection of mice infected with Plasmodium berghei by Bacillus thuringiensis crystal proteins,” Parasitology Research, vol. 92, no. 1, pp. 53–57, 2004.
[27]
D. Hinode, M. Yokoyama, S. Tanabe, M. Yoshioka, and R. Nakamura, “Antigenic properties of the GroEL-like protein of Campylobacter rectus,” Oral Microbiology and Immunology, vol. 17, no. 1, pp. 16–21, 2002.
[28]
J. Peters, M. Peters, F. Lottspeich, W. Sch？fer, and W. Baumeister, “Nucleotide sequence analysis of the gene encoding the Deinococcus radiodurans surface protein, derived amino acid sequence, and complementary protein chemical studies,” Journal of Bacteriology, vol. 169, no. 11, pp. 5216–5223, 1987.
[29]
D. J. Müller, W. Baumeister, and A. Engel, “Conformational change of the hexagonally packed intermediate layer of Deinococcus radiodurans monitored by atomic force microscopy,” Journal of Bacteriology, vol. 178, no. 11, pp. 3025–3030, 1996.
[30]
H. Rothfuss, J. C. Lara, A. K. Schmid, and M. E. Lidstrom, “Involvement of the S-layer proteins Hpi and SlpA in the maintenance of cell envelope integrity in Deinococcus radiodurans R1,” Microbiology, vol. 152, no. 9, pp. 2779–2787, 2006.
[31]
M. Jarosch, E. M. Egelseer, D. Mattanovich, U. B. Sleytr, and M. Sára, “S-layer gene sbsC of Bacillus stearothermaphilus ATCC 12980: molecular characterization and heterologous expression in Escherichia coli,” Microbiology, vol. 146, no. 2, pp. 273–281, 2000.
[32]
R. Novotny, C. Sch？ffer, J. Strauss, and P. Messner, “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, vol. 150, no. 4, pp. 953–965, 2004.
[33]
E. M. Egelseer, T. Danhorn, M. Pleschberger, C. Hotzy, U. B. Sleytr, and M. Sára, “Characterization of an S-layer glycoprotein produced in the course of S-layer variation of Bacillus stearothermophilus ATCC 12980 and sequencing and cloning of the sbsD gene encoding the protein moiety,” Archives of Microbiology, vol. 177, no. 1, pp. 70–80, 2001.
[34]
C. Sch？ffer, T. Wugeditsch, H. K？hlig, A. Scheberl, S. Zayni, and P. Messner, “The surface layer (S-layer) glycoprotein of Geobacillus stearothermophilus NRS 2004/3a. Analysis of its glycosylation,” The Journal of Biological Chemistry, vol. 277, no. 8, pp. 6230–6239, 2002.
[35]
K. Steiner, R. Novotny, and R. Novotny, “Molecular basis of S-layer glycoprotein glycan biosynthesis in Geobacillus stearothermophilus,” The Journal of Biological Chemistry, vol. 283, no. 30, pp. 21120–21133, 2008.
[36]
C. Sch？ffer, W. L. Franck, A. Scheberl, P. Kosma, T. R. McDermott, and P. Messner, “Classification of isolates from locations in Austria and Yellowstone National Park as Geobacillus tepidamans sp. nov,” International Journal of Systematic and Evolutionary Microbiology, vol. 54, no. 6, pp. 2361–2368, 2004.
[37]
H. K？hlig, D. Kolarich, S. Zayni, A. Scheberl, P. Kosma, C. Sch？ffer, and P. Messner, “N-acetylmuramic acid as capping element of α-D-fucose-containing S-layer glycoprotein glycans from Geobacillus tepidamans GS5- ,” The Journal of Biological Chemistry, vol. 280, no. 21, pp. 20292–20299, 2005.
[38]
S. Zayni, K. Steiner, A. Pf？stl, A. Hofinger, P. Kosma, C. Sch？ffer, and P. Messner, “The dTDP-4-dehydro-6-deoxyglucose reductase encoding fcd gene is part of the surface layer glycoprotein glycosylation gene cluster of Geobacillus tepidamans GS5- ,” Glycobiology, vol. 17, no. 4, pp. 433–443, 2007.
[39]
N. Shen and R. M. Weiner, “Isolation and characterization of S-layer proteins from a vent prosthecate bacterium,” Microbios, vol. 93, no. 374, pp. 7–16, 1998.
[40]
A. M？schl, C. Sch？ffer, U. B. Sleytr, P. Messner, R. Christian, and G. Schulz, “Characterization of the S-layer glycoproteins of two lactobacilli,” in Advances in Bacterial Paracrystalline Surface Layers, T. J. Beveridge and S. F. Koval, Eds., pp. 281–284, Plenum Press, New York, NY, USA, 1993.
[41]
N. Mozes and S. Lortal, “X-ray photoelectron spectroscopy and biochemical analysis of the surface of Lactobacillus helveticus ATCC 12046,” Microbiology, vol. 141, no. 1, pp. 11–19, 1995.
[42]
G. L. Garrote, L. Delfederico, R. Bibiloni, A. G. Abraham, P. F. Pérez, L. Semorile, and G. L. De Antoni, “Lactobacilli isolated from kefir grains: evidence of the presence of S-layer proteins,” Journal of Dairy Research, vol. 71, no. 2, pp. 222–230, 2004.
[43]
P. Mobili, M. á. Serradell, S. A. Trejo, F. X. Avilés Puigvert, A. G. Abraham, and G. L. De Antoni, “Heterogeneity of S-layer proteins from aggregating and non-aggregating LactoBacillus kefir strains,” Antonie van Leeuwenhoek, vol. 95, no. 4, pp. 363–372, 2009.
[44]
V. N. Khmelenina, M. G. Kalyuzhnaya, V. G. Sakharovsky, N. E. Snzina, Y. A. Trotsenko, and G. Gottschalk, “Osmoadaptation in halophilic and alkaliphilic methanotrophs,” Archives of Microbiology, vol. 172, no. 5, pp. 321–329, 1999.
[45]
E. Altman, J.-R. Brisson, P. Messner, and U. B. Sleytr, “Chemical characterization of the regularly arranged surface layer glycoprotein of Bacillus alvei CCM 2051,” Biochemistry and Cell Biology, vol. 69, no. 1, pp. 72–78, 1990.
[46]
P. Messner, R. Christian, C. Neuninger, and G. Schulz, “Similarity of “core” structures in two different glycans of tyrosine- linked eubacterial S-layer glycoproteins,” Journal of Bacteriology, vol. 177, no. 8, pp. 2188–2193, 1995.
[47]
K. Zarschler, B. Janesch, S. Zayni, C. Sch？ffer, and P. Messner, “Construction of a gene knockout system for application in Paenibacillus alvei CCM , exemplified by the S-layer glycan biosynthesis initiation enzyme WsfP,” Applied and Environmental Microbiology, vol. 75, no. 10, pp. 3077–3085, 2009.
[48]
K. Zarschler, B. Janesch, M. Pabst, F. Altmann, P. Messner, and C. Sch？ffer, “Protein tyrosine O-glycosylation—a rather unexplored prokaryotic glycosylation system,” Glycobiology, vol. 20, no. 6, pp. 787–798, 2010.
[49]
L. O. Severina, A. A. Senyushkin, and G. I. Karavaiko, “The structure and chemical composition of the S-layer in representatives of the genus Sulfobacillus,” Microbiology (Moscow), vol. 64, no. 3, pp. 280–283, 1995.
[50]
B. Brahamsha, “An abundant cell-surface polypeptide is required for swimming by the nonflagellated marine cyanobacterium Synechococcus,” Proceedings of the National Academy of Sciences of the United States of America, vol. 93, no. 13, pp. 6504–6509, 1996.
[51]
J. McCarren, J. Heuser, R. Roth, N. Yamada, M. Martone, and B. Brahamsha, “Inactivation of swmA results in the loss of an outer cell layer in a swimming Synechococcus strain,” Journal of Bacteriology, vol. 187, no. 1, pp. 224–230, 2005.
[52]
N. Higuchi, Y. Murakami, K. Moriguchi, N. Ohno, H. Nakamura, and F. Yoshimura, “Localization of major, high molecular weight proteins in Bacteroides forsythus,” Microbiology and Immunology, vol. 44, no. 9, pp. 777–780, 2000.
[53]
M. Sabet, S.-W. Lee, R. K. Nauman, T. Sims, and H.-S. Um, “The surface (S-) layer is a virulence factor of Bacteroides forsythus,” Microbiology, vol. 149, no. 12, pp. 3617–3627, 2003.
[54]
J. Peters, M. Peters, F. Lottspeich, and W. Baumeister, “S-layer protein gene of Acetogenium kivui: cloning and expression in Escherichia coli and determination of the nucleotide sequence,” Journal of Bacteriology, vol. 171, no. 11, pp. 6307–6315, 1989.
[55]
R. Christian, P. Messner, C. Weiner, U. B. Sleytr, and G. Schulz, “Structure of a glycan from the surface-layer glycoprotein of Clostridium thermohydrosulfuricum strain L111-69,” Carbohydrate Research, vol. 176, no. 1, pp. 160–163, 1988.
[56]
K. Bock, J. Schuster-Kolbe, and J. Schuster-Kolbe, “Primary structure of the O-glycosidically linked glycan chain of the crystalline surface layer glycoprotein of Thermoanaerobacter thermohydrosulfuricus L111-69. Galactosyl tyrosine as a novel linkage unit,” The Journal of Biological Chemistry, vol. 269, no. 10, pp. 7137–7144, 1994.
[57]
P. Messner, R. Christian, J. Kolbe, G. Schulz, and U. B. Sleytr, “Analysis of a novel linkage unit of O-linked carbohydrates from the crystalline surface layer glycoprotein of Clostridium thermohydrosulfuricum S102-70,” Journal of Bacteriology, vol. 174, no. 7, pp. 2236–2240, 1992.
[58]
R. Christian, G. Schulz, J. Schuster-Kolbe, G. Allmaier, E. R. Schmid, U. B. Sleytr, and P. Messner, “Complete structure of the tyrosine-linked saccharide moiety from the surface layer glycoprotein of Clostridium thermohydrosulfuricum S102-70,” Journal of Bacteriology, vol. 175, no. 5, pp. 1250–1256, 1993.
[59]
E. Altman, J.-R. Brisson, S. M. Gagne, J. Kolbe, P. Messner, and U. B. Sleytr, “Structure of the glycan chain from the surface layer glycoprotein of Clostridium thermohydrosulfuricum L77-66,” Biochimica et Biophysica Acta, vol. 1117, no. 1, pp. 71–77, 1992.
[60]
E. Altman, C. Sch？ffer, J.-R. Brisson, and P. Messner, “Characterization of the glycan structure of a major glycopeptide from the surface layer glycoprotein of Clostridium thermosaccharolyticum E207-71,” European Journal of Biochemistry, vol. 229, no. 1, pp. 308–315, 1995.
[61]
C. Sch？ffer, K. Dietrich, B. Unger, A. Scheber, F. A. Rainey, H. K？hlig, and P. Messner, “A novel type of carbohydrate-protein linkage region in the tyrosine-bound S-layer glycan of Thermoanaerobacterium thermosaccharolyticum D120-70,” European Journal of Biochemistry, vol. 267, no. 17, pp. 5482–5492, 2000.
[62]
E. Brechtel, M. Matuschek, A. Hellberg, E. M. Egelseer, R. Schmid, and H. Bahl, “Cell wall of Thermoanaerobacterium thermosulfurigenes EM1: isolation of its components and attachment of the xylanase XynA,” Archives of Microbiology, vol. 171, no. 3, pp. 159–165, 1999.
[63]
P. Messner, “Prokaryotic protein glycosylation is rapidly expanding from “curiosity” to “ubiquity”,” ChemBioChem, vol. 10, no. 13, pp. 2151–2154, 2009.
[64]
P. Messner, E. Egelseer, U. B. Sleytr, and C. Sch？ffer, “Surface layer glycoproteins and secondary cell wall polymers,” in Microbial Glycobiology: Structures, Relevance and Applications, A. P. Moran, P. J. Brennan, O. Holst, and M. von Itzstein, Eds., pp. 109–128, Academic Press, Elsevier, San Diego, Calif, USA, 2009.
[65]
C. R. H. Raetz and C. Whitfield, “Lipopolysaccharide endotoxins,” Annual Review of Biochemistry, vol. 71, pp. 635–700, 2002.
[66]
P. Messner and C. Sch？ffer, “Prokaryotic glycoproteins,” in Progress in the Chemistry of Organic Natural Products, W. Herz, H. Falk, and G. W. Kirby, Eds., vol. 85, pp. 51–124, Springer, Wien, Austria, 2003.
[67]
C. Sch？ffer, N. Müller, R. Christian, M. Graninger, T. Wugeditsch, A. Scheberl, and P. Messner, “Complete glycan structure of the S-layer glycoprotein of Aneurinibacillus thermoaerophilus GS4-97,” Glycobiology, vol. 9, no. 4, pp. 407–414, 1999.
[68]
C. Whitfield, “Polymerases: glycan chain-length control,” Nature Chemical Biology, vol. 6, no. 6, pp. 403–404, 2010.
[69]
T. Wugeditsch, N. E. Zachara, M. Puchberger, P. Kosma, A. A. Gooley, and P. Messner, “Structural heterogeneity in the core oligosaccharide of the S-layer glycoprotein from Aneurinibacillus thermoaerophilus DSM 10155,” Glycobiology, vol. 9, no. 8, pp. 787–795, 1999.
[70]
C. Sch？ffer, T. Wugeditsch, C. Neuninger, and P. Messner, “Are S-layer glycoproteins and lipopolysaccharides related?” Microbial Drug Resistance, vol. 2, no. 1, pp. 17–23, 1996.
[71]
K. Steiner, G. Pohlentz, K. Dreisewerd, S. Berkenkamp, P. Messner, J. Peter-Katalini？, and C. Sch？ffer, “New insights into the glycosylation of the surface layer protein SgsE from Geobacillus stearothermophilus NRS 2004/3a,” Journal of Bacteriology, vol. 188, no. 22, pp. 7914–7921, 2006.
[72]
W. Keenleyside and C. Whitfield, “Genetics and biosynthesis of lipopolysaccharide O antigens,” in Endotoxin in Health and Disease, H. Brade, S. M. Opal, S. N. Vogel, and D.C. Morrison, Eds., pp. 331–358, Marcel Dekker, New York, NY, USA, 1999.
[73]
I. W. Sutherland, “Biosynthesis and composition of gram-negative bacterial extracellular and wall polysaccharides,” Annual Review of Microbiology, vol. 39, pp. 243–270, 1985.
[74]
C. Whitfield and M. A. Valvano, “Biosynthesis and expression of cell-surface polysaccharides in gram-negative bacteria,” Advances in Microbial Physiology, vol. 35, pp. 135–246, 1993.
[75]
M.-F. Giraud and J. H. Naismith, “The rhamnose pathway,” Current Opinion in Structural Biology, vol. 10, no. 6, pp. 687–696, 2000.
[76]
G. Samuel and P. Reeves, “Biosynthesis of O-antigens: genes and pathways involved in nucleotide sugar precursor synthesis and O-antigen assembly,” Carbohydrate Research, vol. 338, no. 23, pp. 2503–2519, 2003.
[77]
S. D. Bentley, D. M. Aanensen, and D. M. Aanensen, “Genetic analysis of the capsular biosynthetic locus from all 90 pneumococcal serotypes,” PLoS Genetics, vol. 2, no. 3, article e31, 2006.
[78]
S. J. Lee, L. K. Romana, and P. R. Reeves, “Sequence and structural analysis of the rfb (O antigen) gene cluster from a group C1 Salmonella enterica strain,” Journal of General Microbiology, vol. 138, no. 9, pp. 1843–1855, 1992.
[79]
T. Kalambaheti, D. M. Bulach, K. Rajakumar, and B. Adler, “Genetic organization of the lipopolysaccharide O-antigen biosynthetic locus of Leptospira borgpetersenii serovar Hardjobovis,” Microbial Pathogenesis, vol. 27, no. 2, pp. 105–117, 1999.
[80]
M. Hobbs and P. R. Reeves, “The JUMPstart sequence: a 39 bp element common to several polysaccharide gene clusters,” Molecular Microbiology, vol. 12, no. 5, pp. 855–856, 1994.
[81]
R. Novotny, H. Berger, T. Schinko, P. Messner, C. Sch？ffer, and J. Strauss, “A temperature-sensitive expression system based on the Geobacillus stearothermophilus NRS 2004/3a sgsE surface-layer gene promoter,” Biotechnology and Applied Biochemistry, vol. 49, no. 1, pp. 35–40, 2008.
[82]
L. Jolly and F. Stingele, “Molecular organization and functionality of exopolysaccharide gene clusters in lactic acid bacteria,” International Dairy Journal, vol. 11, no. 9, pp. 733–745, 2001.
[83]
K. Steiner, R. Novotny, and R. Novotny, “Functional characterization of the initiation enzyme of S-layer glycoprotein glycan biosynthesis in Geobacillus stearothermophilus NRS 2004/3a,” Journal of Bacteriology, vol. 189, no. 7, pp. 2590–2598, 2007.
[84]
L. Wang, D. Liu, and P. R. Reeves, “C-terminal half of Salmonella enterica WbaP (RfbP) is the galactosyl-1-phosphate transferase domain catalyzing the first step of O-antigen synthesis,” Journal of Bacteriology, vol. 178, no. 9, pp. 2598–2604, 1996.
[85]
M. S. Saldías, K. Patel, C. L. Marolda, M. Bittner, I. Contreras, and M. A. Valvano, “Distinct functional domains of the Salmonella enterica WbaP transferase that is involved in the initiation reaction for synthesis of the O antigen subunit,” Microbiology, vol. 154, no. 2, pp. 440–453, 2008.
[86]
B. R. Clarke, L. Cuthbertson, and C. Whitfield, “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,” The Journal of Biological Chemistry, vol. 279, no. 34, pp. 35709–35718, 2004.
[87]
W. Wang, A. V. Perepelov, and A. V. Perepelov, “A group of Escherichia coli and Salmonella enterica O antigens sharing a common backbone,” Microbiology, vol. 153, no. 7, pp. 2159–2167, 2007.
[88]
G. E. Allison and N. K. Verma, “Serotype-converting bacteriophages and O-antigen modification in Shigella flexneri,” Trends in Microbiology, vol. 8, no. 1, pp. 17–23, 2000.
[89]
D. Bronner, B. R. Clarke, and C. Whitfield, “Identification of an ATP-binding cassette transport system required for translocation of lipopolysaccharide O-antigen side-chains across the cytoplasmic membrane of Klebsiella pneumoniae serotype O1,” Molecular Microbiology, vol. 14, no. 3, pp. 505–519, 1994.
[90]
L. Cuthbertson, J. Powers, and C. Whitfield, “The C-terminal domain of the nucleotide-binding domain protein Wzt determines substrate specificity in the ATP-binding cassette transporter for the lipopolysaccharide O-antigens in Escherichia coli serotypes O8 and O9a,” The Journal of Biological Chemistry, vol. 280, no. 34, pp. 30310–30319, 2005.
[91]
L. Cuthbertson, M. S. Kimber, and C. Whitfield, “Substrate binding by a bacterial ABC transporter involved in polysaccharide export,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 49, pp. 19529–19534, 2007.
[92]
A. Faridmoayer, M. A. Fentabil, D. C. Mills, J. S. Klassen, and M. F. Feldman, “Functional characterization of bacterial oligosaccharyltransferases involved in O-linked protein glycosylation,” Journal of Bacteriology, vol. 189, no. 22, pp. 8088–8098, 2007.
[93]
A. Faridmoayer, M. A. Fentabil, M. F. Haurat, W. Yi, R. Woodward, P. G. Wang, and M. F. Feldman, “Extreme substrate promiscuity of the Neisseria oligosaccharyl transferase involved in protein O-glycosylation,” The Journal of Biological Chemistry, vol. 283, no. 50, pp. 34596–34604, 2008.
[94]
M. Wacker, M. F. Feldman, and M. F. Feldman, “Substrate specificity of bacterial oligosaccharyltransferase suggests a common transfer mechanism for the bacterial and eukaryotic systems,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 18, pp. 7088–7093, 2006.
[95]
N. Maita, J. Nyirenda, M. Igura, J. Kamishikiryo, and D. Kohda, “Comparative structural biology of eubacterial and archaeal oligosaccharyltransferases,” The Journal of Biological Chemistry, vol. 285, no. 7, pp. 4941–4950, 2010.
[96]
P. M. Power, K. L. Seib, and M. P. Jennings, “Pilin glycosylation in Neisseria meningitidis occurs by a similar pathway to wzy-dependent O-antigen biosynthesis in Escherichia coli,” Biochemical and Biophysical Research Communications, vol. 347, no. 4, pp. 904–908, 2006.
[97]
G. L. Blatch and M. L？ssle, “The tetratricopeptide repeat: a structural motif mediating protein-protein interactions,” BioEssays, vol. 21, no. 11, pp. 932–939, 1999.
[98]
L. D. D'Andrea and L. Regan, “TPR proteins: the versatile helix,” Trends in Biochemical Sciences, vol. 28, no. 12, pp. 655–662, 2003.
[99]
C. Whitfield and I. L. Mainprize, “TPR motifs: hallmarks of a new polysaccharide export scaffold,” Structure, vol. 18, no. 2, pp. 151–153, 2010.
[100]
N. Kido, T. Sugiyama, T. Yokochi, H. Kobayashi, and Y. Okawa, “Synthesis of Escherichia coli O9a polysaccharide requires the participation of two domains of WbdA, a mannosyltransferase encoded within the gene cluster,” Molecular Microbiology, vol. 27, no. 6, pp. 1213–1221, 1998.
[101]
B. R. Clarke, L. K. Greenfield, C. Bouwman, and C. Whitfield, “Coordination of polymerization, chain termination, and export in assembly of the Escherichia coli lipopolysaccharide O9a antigen in an ATP-binding cassette transporter-dependent pathway,” The Journal of Biological Chemistry, vol. 284, no. 44, pp. 30662–30672, 2009.
[102]
A. Pfoestl, A. Hofinger, P. Kosma, and P. Messner, “Biosynthesis of dTDP-3-acetamido-3,6-dideoxy-α-D-galactose in Aneurinibacillus thermoaerophilus L420- ,” The Journal of Biological Chemistry, vol. 278, no. 29, pp. 26410–26417, 2003.
[103]
M. L. Davis, J. B. Thoden, and H. M. Holden, “The X-ray structure of dTDP-4-keto-6-deoxy-D-glucose-3,4-ketoisomerase,” The Journal of Biological Chemistry, vol. 282, no. 26, pp. 19227–19236, 2007.
[104]
A. Pf？stl, S. Zayni, A. Hofinger, P. Kosma, C. Sch？ffer, and P. Messner, “Biosynthesis of dTDP-3-acetamido-3,6-dideoxy-α-D-glucose,” Biochemical Journal, vol. 410, no. 1, pp. 187–194, 2008.
[105]
J. B. Thoden, C. Sch？ffer, P. Messner, and H. M. Holden, “Structural analysis of QdtB, an aminotransferase required for the biosynthesis of dTDP-3-acetamido-3,6-dideoxy-α-D-glucose,” Biochemistry, vol. 48, no. 7, pp. 1553–1561, 2009.
[106]
J. B. Thoden, P. D. Cook, C. Sch？ffer, P. Messner, and H. M. Holden, “Structural and functional studies of QdtC: an N-acetyltransferase required for the biosynthesis of dTDP-3-acetamido-3,6-dideoxy-R-D-glucose,” Biochemistry, vol. 48, no. 12, pp. 2699–2709, 2009.
[107]
E. S. Rangarajan, K. M. Ruane, and K. M. Ruane, “Structure and active site residues of PglD, an N-acetyltransferase from the bacillosamine synthetic pathway required for N-glycan synthesis in Campylobacter jejuni,” Biochemistry, vol. 47, no. 7, pp. 1827–1836, 2008.
[108]
N. B. Olivier and B. Imperiali, “Crystal structure and catalytic mechanism of PglD from Campylobacter jejuni,” The Journal of Biological Chemistry, vol. 283, no. 41, pp. 27937–27946, 2008.
[109]
K. Steiner, A. Wojciechowska, C. Sch？ffer, and J. H. Naismith, “Purification, crystallization and preliminary crystallographic analysis of WsaF, an essential rhamnosyltransferase from Geobacillus stearothermophilus,” Acta Crystallographica Section F, vol. 64, no. 12, pp. 1163–1165, 2008.
[110]
K. Steiner, G. Hagelueken, P. Messner, C. Sch？ffer, and J. H. Naismith, “Structural basis of substrate binding in WsaF, a rhamnosyltransferase from Geobacillus stearothermophilus,” Journal of Molecular Biology, vol. 397, no. 2, pp. 436–447, 2010.
[111]
L. L. Lairson, B. Henrissat, G. J. Davies, and S. G. Withers, “Glycosyl transferases: structures, functions, and mechanisms,” Annual Review of Biochemistry, vol. 77, pp. 521–555, 2008.
[112]
M. Graninger, B. Kneidinger, K. Bruno, A. Scheberl, and P. Messner, “Homologs of the Rml enzymes from Salmonella enterica are responsible for dTDP-β-L-rhamnose biosynthesis in the gram-positive thermophile Aneurinibacillus thermoaerophilus DSM 10155,” Applied and Environmental Microbiology, vol. 68, no. 8, pp. 3708–3715, 2002.
[113]
U. B. Sleytr, E.-M. Egelseer, N. Ilk, et al., “Nanobiotechnological applications of S layers,” in Prokaryotic Cell Wall Compounds—Structure and Biochemistry, H. K？nig, H. Claus, and A. Varma, Eds., pp. 459–481, Springer, Heidelberg, Germany, 2010.
