1887

Abstract

Summary: Bacteria synthesize and secrete an array of complex carbohydrates including exopolysaccharides (EPSs), capsular polysaccharides (CPSs), lipopolysaccharides (LPSs), lipo-oligosaccharides (LOSs) and teichoic acids (TCAs). We have analysed the families of homologous proteins that appear to mediate excretion of complex carbohydrates into or across the bacterial cell envelope. Two principal families of cytoplasmic-membrane transport systems appear to drive polysaccharide export: polysaccharide-specific transport (PST) systems and ATP-binding cassette-2 (ABC-2) systems. We present evidence that the secretion of CPSs and EPSs, but not of LPSs, LOSs or TCAs via a PST or ABC-2 system requires the presence of a cytoplasmic-membrane-periplasmic auxiliary protein (MPA1 or MPA2, respectively) in both Gram-negative and Gram-positive bacteria as well as an outer-membrane auxiliary (OMA) protein in Gram-negative bacteria. While all OMA proteins are included within a single family, MPA1 and MPA2 family proteins are not demonstrably homologous to each other, even though they share common topological features. Moreover, MPA1 family proteins (which function with PST systems), but not MPA2 family proteins (which function with ABC-2 systems), possess cytoplasmic ATP-binding domains that may either exist as separate polypeptide chains (for those from Gram-positive bacteria) or constitute the C-terminal domain of the MPA1 polypeptide chain (for those from Gram-negative bacteria). The sizes, substrate specificities and regions of relative conservation and hydrophobicity are defined allowing functional and structural predictions as well as delineation of family-specific sequence motifs. Each family is characterized phylogenetically.

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1997-08-01
2021-05-13
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References

  1. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D.J. 1990; Basic local alignment search tool. J Mol Biol 215:403–410
    [Google Scholar]
  2. Bailey T. L., Elkan C. 1994; Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proceedings of the Second International Conference on Intelligent Systems for Molecular Biology pp. 28–36 Menlo Park, CA: AAAI Press;
    [Google Scholar]
  3. Bairoch A. 1992; prosite: a dictionary of sites and patterns in proteins. Nucleic Acids Res 20:2013–2018
    [Google Scholar]
  4. Bartlett D. H., Wright M. E., Silverman M. 1988; Variable expression of extracellular polysaccharide in the marine bacterium Pseudomonas atlantica is controlled by genome rearrangement. Proc Natl Acad Sci USA 85:3923–3927
    [Google Scholar]
  5. Bayer M. E. 1968; Areas of adhesion between wall and membrane of Escherichia coli. . J Gen Microbiol 53:395–404
    [Google Scholar]
  6. Berger E. A., Heppel L. A. 1974; Different mechanisms of energy coupling for the shock-sensitive and shock-resistant amino acid permeases of Escherichia coli. . J Biol Chem 249:7747–7755
    [Google Scholar]
  7. Betlach M. R., Capage M. A., Doherty D. H., Hassler R. A., Henderson N. M., van der Slice R. W., Marrelli J. D., Ward M. B. 1987; Genetically engineered polymers: manipulation of xanthan biosynthesis. . In Industrial Polysaccharides: Genetic Engineering, Structure/Property Relations and Applications pp. 35–50 . Edited by Yalpani M. Amsterdam: Elsevier Science Publishers;
    [Google Scholar]
  8. Bik E. M., Bunschoten A. E., Gouw R. D., Mooi F. R. 1995; Genesis of the novel epidemic Vibrio cholerae O139 strain: evidence for horizontal transfer of genes involved in polysaccharide synthesis. EMBO J 14:209–216
    [Google Scholar]
  9. Boulnois G. J., Jann K. 1989; Bacterial polysaccharide capsule synthesis, export and evolution of structural diversity. Mol Microbiol 3:1819–1823
    [Google Scholar]
  10. Boulnois G. J., Roberts I. S. 1990; Genetics of capsular polysaccharide production in bacteria. Curr Top Microbiol Immunol 150:1–20
    [Google Scholar]
  11. Bronner D., Sieberth V., Pazzani C., Roberts I. S., Boulnois G. J., Jann B., Jann K. 1993a; Expression of the capsular K5 polysaccharide of Escherichia coli: biochemical and electron microscopic analyses of mutants with defects in region 1 of the K5 gene cluster. J Bacteriol 175:5984–5992
    [Google Scholar]
  12. Bronner D., Sieberth V., Pazzani C., Smith A., Boulnois G., Roberts I., Jann B., Jann K. 1993b; Synthesis of the K5 (group II) capsular polysaccharide in transport-deficient recombinant Escherichia coli. . FEMS Microbiol Lett 113:279–284
    [Google Scholar]
  13. Bugert P., Geider K. 1995; Molecular analysis of the ams operon required for exopolysaccharide synthesis of Erwinia amylovora. . Mol Microbiol 15:917–933
    [Google Scholar]
  14. Capage M. A., Doherty D. H., Betlach M. R., van der Slice R. 1987 Recombinant-DNA mediated production of xanthan gumPatent International Publication No. WO87/05938
    [Google Scholar]
  15. Chou P. Y., Fasman G. D. 1978; Empirical prediction of protein conformation. Annu Rev Biochem 47:251–276
    [Google Scholar]
  16. Dayhoff M. O., Barker W. C., Hunt L. T. 1983; Establishing homologies in protein sequences. Methods Enzymol 91:524–545
    [Google Scholar]
  17. Devereux J., Haeberli P., Smithies O. 1984; A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 12:387–395
    [Google Scholar]
  18. Dey S., Rosen B. P. 1995; Dual mode of energy coupling by the oxyanion-translocating ArsB protein. J Bacteriol 177:385–389
    [Google Scholar]
  19. Dinh T., Paulsen I. T., Saier M. H. Jr 1994; A family of extracytoplasmic proteins that allow transport of large molecules across the outer membranes of Gram-negative bacteria. J Bacteriol 176:3825–3831
    [Google Scholar]
  20. Dong Q., Mergeay M. 1994; Czc/Cnr efflux: a three-component chemiosmotic antiport pathway with a 12-transmembrane-helix protein. Mol Microbiol 14:185–187
    [Google Scholar]
  21. Dorman C. J. 1995; DNA topology and the global control of bacterial gene expression: implications for the regulation of virulence gene expression. Microbiology 141:1271–1280
    [Google Scholar]
  22. Dybvig K. 1993; DNA rearrangements and phenotypic switching in prokaryotes. Mol Microbiol 10:465–471
    [Google Scholar]
  23. Fath M.J., Kolter R. 1993; ABC transporters: bacterial exporters. Microbiol Rev 57:995–1017
    [Google Scholar]
  24. Feng D.-F., Doolittle R. F. 1990; Progressive alignment and phylogenetic tree construction of protein sequences. Methods Enzymol 183:375–387
    [Google Scholar]
  25. Frosch M., Weisgerber C., Meyer T. F. 1989; Molecular characterization and expression in Escherichia coli of the gene complex encoding the polysaccharide capsule of Neisseria meningitidis group B. Proc Natl Acad Sci USA 86:1669–1673
    [Google Scholar]
  26. Frosch M., Edwards U., Bousset K., Krauße B., Weisgerber C. 1991; Evidence for a common molecular origin of the capsule gene loci in Gram-negative bacteria expressing group II capsular polysaccharides. Mol Microbiol 5:1251–1263
    [Google Scholar]
  27. Frosch M, Müller D.,, Bousset K., Müller A. 1992; Conserved outer membrane protein of Neisseria meningitidis involved in capsule expression. Infect Immun 60:798–803
    [Google Scholar]
  28. Garnier J., Osguthorpe D. J., Robson B. 1978; Analysis of the accuracy and implications of simple methods for predicting the secondary structure of globular proteins. J Mol Biol 120:97–120
    [Google Scholar]
  29. Glucksmann M. A., Reuber T. L., Walker G. C. 1993; Genes needed for the modification, polymerization, export, and processing of succinoglycan by Rhizobium meliloti: a model for succinoglycan biosynthesis. J Bacteriol 175:7045–7055
    [Google Scholar]
  30. Guidolin A., Morona J. K., Morona R., Hansman D., Paton J. C. 1994; Nucleotide sequence analysis of genes essential for capsular polysaccharide biosynthesis in Streptococcus pneumoniae Type 19F. Infect Immun 62:5384–5396
    [Google Scholar]
  31. Hashimoto Y., Li N., Yokoyama H., Ezaki T. 1993; Complete nucleotide sequence and molecular characterization of ViaB region encoding Vi antigen in Salmonella typhi. . J Bacteriol 175:4456–4465
    [Google Scholar]
  32. von Heijne G. 1992; Membrane protein structure prediction. Hydrophobicity analysis and the positive-inside rule. J Mol Biol 225:487–494
    [Google Scholar]
  33. Higgins C. F. 1992; ABC transporters: from microorganisms to man. Annu Rev Cell Biol 8:67–113
    [Google Scholar]
  34. Hoischen C., Pitaknarongphorn S., Reizer J., Levin J., Tomich J. M., Saier M. H. Jr 1996; Involvement of the central loop of the lactose permease of Escherichia coli in its allosteric regulation by the glucose-specific Enzyme IIA of the phosphoenolpyruvate-dependent phosphotransferase system. J Bacteriol 178:6082–6086
    [Google Scholar]
  35. Hornick R. B., Greisman S. E., Woodward T. E., DuPont H. L., Dawkins A. T., Snyder M. J. 1970; Typhoid fever: pathogenesis and immunologic control. N Engl J Med 283:739–746
    [Google Scholar]
  36. Huang J., Schell M. 1995; Molecular characterization of the eps gene cluster of Pseudomonas solanacearum and its transcriptional regulation at a single promoter. Mol Microbiol 16:977–989
    [Google Scholar]
  37. Jann B., Jann K. 1990; Structure and biosynthesis of the capsular antigens of Escherichia coli. . Curr Top Microbiol Immunol 150:19–42
    [Google Scholar]
  38. Jann K., Jann B. 1984; Structure and biosynthesis of O-antigens. . In Handbook of Endotoxin, Vol. 1 Chemistry of Endotoxin , pp. 138–186 . Edited by Rietsche E. T. Amsterdam: Elsevier Science Publishers;
    [Google Scholar]
  39. Jann K., Pillat M., Weisgerber C., Shibaev V. N., Torgov V. I. 1985; Biosynthesis of the 09 antigen of Escherichia coli. Synthetic glycosyldiphosphomoraprenols as probes for requirement of mannose acceptors. Eur J Biochem 151:393–397
    [Google Scholar]
  40. Kido N., Torgov V. I., Sugiyama T., Uchiya K., Sugihara H., Komatsu T., Kato N., Jann K. 1995; Expression of the O9 polysaccharide of Escherichia coli: sequencing of the E. coli O9 rfb gene cluster, characterization of mannosyl transferases, and evidence for an ATP-binding cassette transport system. J Bacteriol 177:2178–2187
    [Google Scholar]
  41. Klena J. D., Schnaitman C. A. 1993; Function of the rfb gene cluster and the rfe gene in the synthesis of O antigen by Shigella dysenteriae 1. Mol Microbiol 9:393–402
    [Google Scholar]
  42. Kroll J. S., Loynds B., Brophy L. M., Moxon E. R. 1990; The bex locus in encapsulated Haemophilus influenzae: a chromosomal region involved in capsule polysaccharide export. Mol Microbiol 4:1853–1862
    [Google Scholar]
  43. Krӧncke K.-D., Boulnois G., Roberts I., Bitter-Suermann D., Golecki J. R., Jann B., Jann K. 1990; Expression of the Escherichia coli K5 capsular antigen: immunoelectron microscopic and biochemical studies with recombinant E. . coli. J Bacteriol 172:1085–1091
    [Google Scholar]
  44. Kuan G., Dassa E., Saurin W., Hofnung M., Saier M. H. Jr 1995; Phylogenetic analyses of the ATP-binding constituents of bacterial extracytoplasmic receptor-dependent ABC-type nutrient uptake permeases. Res Microbiol 146:271–278
    [Google Scholar]
  45. Kyte J., Doolittle R. F. 1982; A simple method for displaying the hydropathic character of a protein. J Mol Biol 157:105–132
    [Google Scholar]
  46. Lazarevic V., Karamata D. 1995; The tagGH operon of Bacillus subtilis 168 encodes a two-component ABC transporter involved in the metabolism of two wall teichoic acids. Mol Microbiol 16:345–355
    [Google Scholar]
  47. Lin W. S., Cunneen T., Lee C. Y. 1994; Sequence analysis and molecular characterization of genes required for the biosynthesis of type 1 capsular polysaccharide in Staphylococcus aureus. . J Bacteriol 176:7005–7016
    [Google Scholar]
  48. Liu D., Cole R. A., Reeves P. R. 1996; An O-antigen function for Wzx (RfbX): a promising candidate for O-unit flippase. J Bacteriol 178:2102–2107
    [Google Scholar]
  49. Long S., Reed J. W., Himawan J., Walker G. C. 1988; Genetic analysis of a cluster of genes required for synthesis of the calcofluor-binding exopolysaccharide of Rhizobium meliloti. . J Bacteriol 170:4239–4248
    [Google Scholar]
  50. McGrath B. C., Osborn M. J. 1991; Evidence for energy-dependent transposition of core lipopolysaccharide across the inner membrane of Salmonella typhimurium. . J Bacteriol 173:3134–3137
    [Google Scholar]
  51. Macpherson D. F., Manning P. A., Morona R. 1995; Genetic analysis of the rfbX gene of Shigella flexneri. . Gene 155:9–17
    [Google Scholar]
  52. Manning P. A., Stroeher U. H., Karageorgos L. E., Morona R. 1995; Putative O-antigen transport genes within the rfb tegion of Vibrio cholerae O1 are homologous to those for capsule transport. Gene 158:1–7
    [Google Scholar]
  53. Morona R., Macpherson D. F., van den Bosch L., Carlin N. I. A., Manning P. A. 1995; Lipopolysaccharide with an altered O-antigen produced in Escherichia coli K-12 harbouring mutated, cloned Shigella flexneri rfb genes. Mol Microbiol 18:209–223
    [Google Scholar]
  54. Mulford C. A., Osborn M. J. 1983; An intermediate step in translocation of lipopolysaccharide to the outer membrane of Salmonella typhimurium. . Proc Natl Acad Sci USA 80:1159–1163
    [Google Scholar]
  55. Pavelka M. S., Jr, Wright L. F., Silver R. P. 1991; Identification of two genes, kpsM and kpsT, in region 3 of the polysialic acid gene cluster of Escherichia coli K12. J Bacteriol 173:4603–4610
    [Google Scholar]
  56. Pearce R., Roberts I. S. 1995; Cloning and analysis of gene clusters for production of the Escherichia coli K10 and K54 antigens: identification of a new group of serA-linked capsule gene clusters. J Bacteriol 177:3992–3997
    [Google Scholar]
  57. Pearson W. R., Lipman D. J. 1988; Improved tools for biological sequence comparison. Proc Natl Acad Sci USA 85:2444–2448
    [Google Scholar]
  58. Reeves P. R. 1992; Variation in O-antigens, niche-specific selection and bacterial populations. FEMS Microbiol Lett 100:509–516
    [Google Scholar]
  59. Reeves P. 1993; Evolution of Salmonella O antigen variation by interspecific gene transfer on a large scale. Trends Genet 9:17–22
    [Google Scholar]
  60. Reizer J., Reizer A., Saier M. H. Jr 1992; A new subfamily of bacterial ABC-type transport systems catalyzing export of drugs and carbohydrates. Protein Sci 1:1326–1332
    [Google Scholar]
  61. Reuber T. L., Walker G. C. 1993; Biosynthesis of succino-glycan, a symbiotically important exopolysaccharide of Rhizobium meliloti. . Cell 74:269–280
    [Google Scholar]
  62. Reuber T. L., Long S., Walker G. C. 1991; Regulation of Rhizobium meliloti exo genes in free-living cells and in planta examined by using TnphoA fusions. J Bacteriol 173:426–434
    [Google Scholar]
  63. Robbins J. D., Robbins J. B. 1984; Re-examination of the protective role of the capsular polysaccharide (Vi antigen) of Salmonella typhi. . J Infect Dis 150:436–449
    [Google Scholar]
  64. Roberts I. S. 1995; Bacterial polysaccharides in sickness and in health. Microbiology 141:2023–2031
    [Google Scholar]
  65. Rosenow C., Esumeh F., Roberts I. S., Jann K. 1995; Characterization and localization of the KpsE protein of Escherichia coli K5, which is involved in polysaccharide export. J Bacteriol 177:1137–1143
    [Google Scholar]
  66. Saier M. H. Jr 1994; Computer-aided analyses of transport protein sequences: gleaning evidence concerning function, structure, biogenesis, and evolution. Microbiol Rev 58:71–93
    [Google Scholar]
  67. Saier M. H. Jr 1996; Phylogenetic approaches to the identification and characterization of protein families and superfamilies. Microb Comp Genomics 1:129–150
    [Google Scholar]
  68. Saier M. H., Jr & Jacobson G. R. 1984 The Molecular Basis of Sex and Differentiation: a Comparative Study of Evolution, Mechanism and Control in Microorganisms New York: Springer;
    [Google Scholar]
  69. Saier M. H., Jr, Tam R., Reizer A., Reizer J. 1994; Two novel families of bacterial membrane proteins concerned with nodulation, cell division and transport. Mol Microbiol 11:841–847
    [Google Scholar]
  70. Schnaitman C. A., Klena J. D. 1993; Genetics of lipopoly-saccharide biosynthesis in enteric bacteria. Microbiol Rev 57:655–682
    [Google Scholar]
  71. Seifert H. S., So M. 1988; Genetic mechanisms of bacterial antigenic variation. Microbiol Rev 52:327–336
    [Google Scholar]
  72. Silver R. P., Aaronson W., Vann W. F. 1987; Translocation of capsular polysaccharides in pathogenic strains of Escherichia coli requires a 60-kilodalton periplasmic protein. J Bacteriol 169:5489–5495
    [Google Scholar]
  73. Smith A. N., Boulnois G. J., Roberts I. S. 1990; Molecular analysis of the Escherichia coli K5 kps locus: identification and characterization of an inner-membrane capsular polysaccharide transport system. Mol Microbiol 4:1863–1869
    [Google Scholar]
  74. Tam R., Saier M. H. Jr 1993; Structural, functional, and evolutionary relationships among extracellular solute-binding receptors of bacteria. Microbiol Rev 57:320–346
    [Google Scholar]
  75. Walker J. E., Saraste M., Runswick M. J., Gay N. J. 1982; Distantly related sequences in the α-and β-subunits of ATP synthase myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J 1:945–951
    [Google Scholar]
  76. Wilson T. H., Yunker P. L., Hansen C. L. 1990; Lactose transport of Escherichia coli resistant to inhibition by the phosphotransferase system. Biochim Biophys Acta 1029:113–116
    [Google Scholar]
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