Genetic diversity of capsular polysaccharide biosynthesis in Klebsiella pneumoniae clinical isolates

Microbiology

Volumn 155, Issue 12, 2009, Pages 4170-4183

  Shu, Hung Yu ^a,b   Fung, Chang Phone ^b,c   Liu, Yen Ming ^d   Wu, Keh Ming ^b,d   Chen, Ying Tsong ^d   Li, Ling Hui ^d   Liu, Tze Tze ^b   Kirby, Ralph ^b   Tsai, Shih Feng ^b,d  

^a CHANG JUNG CHRISTIAN UNIVERSITY   (Taiwan)

^b NATIONAL YANG MING UNIVERSITY   (Taiwan)

^c TAIPEI VETERANS GENERAL HOSPITAL   (Taiwan)

^d NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL POLYSACCHARIDE; BACTERIAL PROTEIN; UNCLASSIFIED DRUG; WBAJ; WBAP;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ARTICLE; BACTERIAL STRAIN; BACTERIUM ISOLATE; CONTROLLED STUDY; DNA BASE COMPOSITION; DNA CONTENT; GENE CLUSTER; GENE EXPRESSION; GENE TRANSFER; GENETIC VARIABILITY; KLEBSIELLA PNEUMONIAE; NONHUMAN; NUCLEOTIDE METABOLISM; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN POLYMERIZATION; PROTEIN PROCESSING; PROTEIN TRANSPORT; SEROTYPE;

BACTERIAL CAPSULES; BASE SEQUENCE; DNA, BACTERIAL; GENE TRANSFER, HORIZONTAL; GENES, BACTERIAL; GENETIC VARIATION; HUMANS; KLEBSIELLA INFECTIONS; KLEBSIELLA PNEUMONIAE; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; RECOMBINATION, GENETIC; SPECIES SPECIFICITY;

BACTERIA (MICROORGANISMS); KLEBSIELLA PNEUMONIAE;

EID: 71449115272     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.029017-0     Document Type: Article

References (73)

1. Albermann, C., Distler, J. & Piepersberg, W. (2000). Preparative synthesis of GDP-β-L-fucose by recombinant enzymes from enterobacterial sources. Glycobiology 10, 875-881.
2. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W. & Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25, 3389-3402.
3. Andrianopoulos, K., Wang, L. & Reeves, P. R. (1998). Identification of the fucose synthetase gene in the colanic acid gene cluster of Escherichia coli K-12. J Bacteriol 180, 998-1001.
4. Arakawa, Y., Wacharotayankun, R., Nagatsuka, T., Ito, H., Kato, N. & Ohta, M. (1995). Genomic organization of the Klebsiella pneumoniae cps region responsible for serotype K2 capsular polysaccharide synthesis in the virulent strain Chedid. J Bacteriol 177, 1788-1796.
5. Bateman, A., Coin, L., Durbin, R., Finn, R. D., Hollich, V., Griffiths-Jones, S., Khanna, A., Marshall, M., Moxon, S. & other authors (2004). The Pfam protein families database. Nucleic Acids Res 32, D138-D141.
6. Beis, K., Collins, R. F., Ford, R. C., Kamis, A. B., Whitfield, C. & Naismith, J. H. (2004). Three-dimensional structure of Wza, the protein required for translocation of group 1 capsular polysaccharide across the outer membrane of Escherichia coli. J Biol Chem 279, 28227-28232.
7. Borodovsky, M. & McIninch, J. (1993). GENMARK: Parallel gene recognition for both DNA strands. Comput Chem 17, 123-133.
8. Breton, C., Bettler, E., Joziasse, D. H., Geremia, R. A. & Imberty, A. (1998). Sequence-function relationships of prokaryotic and eukaryotic galactosyltransferases. J Biochem 123, 1000-1009.
9. Brisse, S., Issenhuth-Jeanjean, S. & Grimont, P. A. (2004). Molecular serotyping of Klebsiella species isolates by restriction of the amplified capsular antigen gene cluster. J Clin Microbiol 42, 3388-3398.
10. Cescutti, P., Osman, S. F., Fett, W. F. & Weisleder, D. (1995). The structure of the acidic exopolysaccharide produced by Pseudomonas "gingeri" strain Pf9. Carbohydr Res 275, 371-379.
11. Chakraborty, A. K., Friebolin, H. & Stirm, S. (1980). Primary structure of the Escherichia coli serotype K30 capsular polysaccharide. J Bacteriol 141, 971-972.
12. Chuang, Y. P., Fang, C. T., Lai, S. Y., Chang, S. C. & Wang, J. T. (2006). Genetic determinants of capsular serotype K1 of Klebsiella pneumoniae causing primary pyogenic liver abscess. J Infect Dis 193, 645-654.
13. Collins, R. F., Beis, K., Clarke, B. R., Ford, R. C., Hulley, M., Naismith, J. H. & Whitfield, C. (2006). Periplasmic protein-protein contacts in the inner membrane protein Wzc form a tetrameric complex required for the assembly of Escherichia coli group 1 capsules. J Biol Chem 281, 2144-2150.
14. 13C NMR characterization and secondary structure of the K2 polysaccharide of Klebsiella pneumoniae strain 52145. Carbohydr Res 340, 2212-2217.
15. Coutinho, P. M., Deleury, E., Davies, G. J. & Henrissat, B. (2003). An evolving hierarchical family classification for glycosyltransferases. J Mol Biol 328, 307-317.
16. Cunneen, M. M. & Reeves, P. R. (2008). Membrane topology of the Salmonella enterica serovar Typhimurium group B O-antigen translocase Wzx. FEMS Microbiol Lett 287, 76-84.
17. DebRoy, C., Fratamico, P. M., Roberts, E., Davis, M. A. & Liu, Y. (2005). Development of PCR assays targeting genes in O-antigen gene clusters for detection and identification of Escherichia coli O45 and O55 serogroups. Appl Environ Microbiol 71, 4919-4924.
18. Delcher, A. L., Harmon, D., Kasif, S., White, O. & Salzberg, S. L. (1999). Improved microbial gene identification with GLIMMER. Nucleic Acids Res 27, 4636-4641.
19. Dong, C., Beis, K., Nesper, J., Brunkan-Lamontagne, A. L., Clarke, B. R., Whitfield, C. & Naismith, J. H. (2006). Wza the translocon for E. coli capsular polysaccharides defines a new class of membrane protein. Nature 444, 226-229.
20. Drummelsmith, J. & Whitfield, C. (1999). Gene products required for surface expression of the capsular form of the group 1 K antigen in Escherichia coli (O9a : K30). Mol Microbiol 31, 1321-1332.
21. Ewing, B. & Green, P. (1998). Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res 8, 186-194.
22. Fang, C. T., Lai, S. Y., Yi, W. C., Hsueh, P. R., Liu, K. L. & Chang, S. C. (2007). Klebsiella pneumoniae genotype K1: an emerging pathogen that causes septic ocular or central nervous system complications from pyogenic liver abscess. Clin Infect Dis 45, 284-293.
23. Finn, R. D., Mistry, J., Schuster-Bockler, B., Griffiths-Jones, S., Hollich, V., Lassmann, T., Moxon, S., Marshall, M., Khanna, A. & other authors (2006). Pfam: clans, web tools and services. Nucleic Acids Res 34, D247-D251.
24. Franco, O. L. & Rigden, D. J. (2003). Fold recognition analysis of glycosyltransferase families: further members of structural superfamilies. Glycobiology 13, 707-712.
25. Fung, C. P., Hu, B. S., Chang, F. Y., Lee, S. C., Kuo, B. I., Ho, M., Siu, L. K. & Liu, C. Y. (2000). A 5-year study of the seroepidemiology of Klebsiella pneumoniae: high prevalence of capsular serotype K1 in Taiwan and implication for vaccine efficacy. J Infect Dis 181, 2075-2079.
26. Fung, C. P., Chang, F. Y., Lee, S. C., Hu, B. S., Kuo, B. I., Liu, C. Y., Ho, M. & Siu, L. K. (2002). A global emerging disease of Klebsiella pneumoniae liver abscess: is serotype K1 an important factor for complicated endophthalmitis? Gut 50, 420-424.
27. Giraud, M. F. & Naismith, J. H. (2000). The rhamnose pathway. Curr Opin Struct Biol 10, 687-696.
28. Gordon, D., Abajian, C. & Green, P. (1998). Consed: a graphical tool for sequence finishing. Genome Res 8, 195-202.
29. Götting, C., Müller, S., Schöttler, M., Schön, S., Prante, C., Brinkmann, T., Kuhn, J. & Kleesiek, K. (2004). Analysis of the DXD motifs in human xylosyltransferase I required for enzyme activity. J Biol Chem 279, 42566-42573.
30. Grangeasse, C., Obadia, B., Mijakovic, I., Deutscher, J., Cozzone, A. J. & Doublet, P. (2003). Autophosphorylation of the Escherichia coli protein kinase Wzc regulates tyrosine phosphorylation of Ugd, a UDP-glucose dehydrogenase. J Biol Chem 278, 39323-39329.
31. Graninger, M., Kneidinger, B., Bruno, K., Scheberl, A. & Messner, P. (2002). 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. Appl Environ Microbiol 68, 3708-3715.
32. Hofmann, K. & Stoffel, W. (1993). TMbase - a database of membrane spanning protein segments. Biol Chem Hoppe Seyler 374, 166.
33. Homonylo, M. K., Wilmot, S. J., Lam, J. S., MacDonald, L. A. & Whitfield, C. (1988). Monoclonal antibodies against the capsular K antigen of Escherichia coli (O9 : K30(A): H12): characterisation and use in analysis of K antigen organisation on the cell surface. Can J Microbiol 34, 1159-1165.
34. Jann, K. & Jann, B. (1997). Capsules of Escherichia coli. In Escherichia coli: Mechanisms of Virulence, pp. 113-143. Edited by M. Sussman. Cambridge, UK: Cambridge University Press.
35. Jiang, S. M., Wang, L. & Reeves, P. R. (2001). Molecular characterization of Streptococcus pneumoniae type 4, 6B, 8, and 18C capsular polysaccharide gene clusters. Infect Immun 69, 1244-1255.
36. Klutts, J. S., Levery, S. B. & Doering, T. L. (2007). A β-1,2-xylosyltransferase from Cryptococcus neoformans defines a new family of glycosyltransferases. J Biol Chem 282, 17890-17899.
37. Kong, F., Wang, W., Tao, J., Wang, L., Wang, Q., Sabananthan, A. & Gilbert, G. L. (2005). A molecular-capsular-type prediction system for 90 Streptococcus pneumoniae serotypes using partial cpsA-cpsB sequencing and wzy- or wzx-specific PCR. J Med Microbiol 54, 351-356.
38. Köplin, R., Wang, G., Hötte, B., Priefer, U. B. & Pühler, A. (1993). A 3.9-kb DNA region of Xanthomonas campestris pv. campestris that is necessary for lipopolysaccharide production encodes a set of enzymes involved in the synthesis of dTDP-rhamnose. J Bacteriol 175, 7786-7792.
39. Laakso, D. H., Homonylo, M. K., Wilmot, S. J. & Whitfield, C. (1988). Transfer and expression of the genetic determinants for O and K antigen synthesis in Escherichia coli O9: K(A)30 and Klebsiella sp. O1:K20, in Escherichia coli K12. Can J Microbiol 34, 987-992.
40. Lai, Y. C., Peng, H. L. & Chang, H. Y. (2003). RmpA2, an activator of capsule biosynthesis in Klebsiella pneumoniae CG43, regulates K2 cps gene expression at the transcriptional level. J Bacteriol 185, 788-800.
41. Lee, R., Monsey, D., Weston, A., Duncan, K., Rithner, C. & McNeil, M. (1996). Enzymatic synthesis of UDP-galactofuranose and an assay for UDP-galactopyranose mutase based on high-performance liquid chromatography. Anal Biochem 242, 1-7.
42. Li, J., Rancour, D. M., Allende, M. L., Worth, C. A., Darling, D. S., Gilbert, J. B., Menon, A. K. & Young, W. W., Jr (2001). The DXD motif is required for GM2 synthase activity but is not critical for nucleotide binding. Glycobiology 11, 217-229.
43. Liu, J. & Mushegian, A. (2003). Three monophyletic superfamilies account for the majority of the known glycosyltransferases. Protein Sci 12, 1418-1431.
44. Liu, D., Haase, A. M., Lindqvist, L., Lindberg, A. A. & Reeves, P. R. (1993). Glycosyl transferases of O-antigen biosynthesis in Salmonella enterica: identification and characterization of transferase genes of groups B, C2, and E1. J Bacteriol 175, 3408-3413.
45. Lukashin, A. V. & Borodovsky, M. (1998). GeneMark.hmm: new solutions for gene finding. Nucleic Acids Res 26, 1107-1115.
46. Ma, Y., Stern, R. J., Scherman, M. S., Vissa, V. D., Yan, W., Jones, V. C., Zhang, F., Franzblau, S. G., Lewis, W. H. & McNeil, M. R. (2001). Drug targeting Mycobacterium tuberculosis cell wall synthesis: genetics of dTDP-rhamnose synthetic enzymes and development of a microtiter plate-based screen for inhibitors of conversion of dTDP-glucose to dTDP-rhamnose. Antimicrob Agents Chemother 45, 1407-1416.
47. Marolda, C. L. & Valvano, M. A. (1996). The GalF protein of Escherichia coli is not a UDP-glucose pyrophosphorylase but interacts with the GalU protein possibly to regulate cellular levels of UDP-glucose. Mol Microbiol 22, 827-840.
48. Mazur, A., Marczak, M., Krol, J. E. & Skorupska, A. (2005). Topological and transcriptional analysis of pssL gene product: a putative Wzx-like exopolysaccharide translocase in Rhizobium leguminosarum bv. trifolii TA1. Arch Microbiol 184, 1-10.
49. Miller, J. H. (1972). Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
50. Mori, M., Ohta, M., Agata, N., Kido, N., Arakawa, Y., Ito, H., Komatsu, T. & Kato, N. (1989). Identification of species and capsular types of Klebsiella clinical isolates, with special reference to Klebsiella planticola. Microbiol Immunol 33, 887-895.
51. Nakhamchik, A., Wilde, C. & Rowe-Magnus, D. A. (2007). Identification of a Wzy polymerase required for group IV capsular polysaccharide and lipopolysaccharide biosynthesis in Vibrio vulnificus. Infect Immun 75, 5550-5558.
52. Nassau, P. M., Martin, S. L., Brown, R. E., Weston, A., Monsey, D., McNeil, M. R. & Duncan, K. (1996). Galactofuranose biosynthesis in Escherichia coli K-12: identification and cloning of UDP-galactopyranose mutase. J Bacteriol 178, 1047-1052.
53. Nelson, K. & Selander, R. K. (1994). Intergeneric transfer and recombination of the 6-phosphogluconate dehydrogenase gene (gnd) in enteric bacteria. Proc Natl Acad Sci U S A 91, 10227-10231.
54. Niemann, H., Chakraborty, A. K., Friebolin, H. & Stirm, S. (1978). Primary structure of the Escherichia coli serotype K42 capsular polysaccharide and its serological identity with the Klebsiella K63 polysaccharide. J Bacteriol 133, 390-391.
55. Olson, S. A. (1994). MacVector: an integrated sequence analysis program for the Macintosh. Methods Mol Biol 25, 195-201.
56. Pan, Y. J., Fang, H. C., Yang, H. C., Lin, T. L., Hsieh, P. F., Tsai, F. C., Keynan, Y. & Wang, J. T. (2008). Capsular polysaccharide synthesis regions in Klebsiella pneumoniae serotype K57 and a new capsular serotype. J Clin Microbiol 46, 2231-2240.
57. Persson, M., Letts, J. A., Hosseini-Maaf, B., Borisova, S. N., Palcic, M. M., Evans, S. V. & Olsson, M. L. (2007). Structural effects of naturally occurring human blood group B galactosyltransferase mutations adjacent to the DXD motif. J Biol Chem 282, 9564-9570.
58. Podschun, R. & Ullmann, U. (1998). Klebsiella spp. as nosocomial pathogens: epidemiology, taxonomy, typing methods, and pathogenicity factors. Clin Microbiol Rev 11, 589-603.
59. Pruitt, K. D., Tatusova, T. & Maglott, D. R. (2007). NCBI reference sequences (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res 35, D61-D65.
60. Rahn, A. & Whitfield, C. (2003). Transcriptional organization and regulation of the Escherichia coli K30 group 1 capsule biosynthesis (cps) gene cluster. Mol Microbiol 47, 1045-1060.
61. Rahn, A., Drummelsmith, J. & Whitfield, C. (1999). Conserved organization in the cps gene clusters for expression of Escherichia coli group 1 K antigens: relationship to the colanic acid biosynthesis locus and the cps genes from Klebsiella pneumoniae. J Bacteriol 181, 2307-2313.
62. Sanders, D. A., Staines, A. G., McMahon, S. A., McNeil, M. R., Whitfield, C. & Naismith, J. H. (2001). UDP-galactopyranose mutase has a novel structure and mechanism. Nat Struct Biol 8, 858-863.
63. Stenutz, R., Erbing, B., Widmalm, G., Jansson, P. E. & Nimmich, W. (1997). The structure of the capsular polysaccharide from Klebsiella type 52, using the computerised approach CASPER and NMR spectroscopy. Carbohydr Res 302, 79-84.
64. Stevenson, G., Andrianopoulos, K., Hobbs, M. & Reeves, P. R. (1996). Organization of the Escherichia coli K-12 gene cluster responsible for production of the extracellular polysaccharide colanic acid. J Bacteriol 178, 4885-4893.
65. Tonetti, M., Sturla, L., Bisso, A., Benatti, U. & De Flora, A. (1996). Synthesis of GDP-L-fucose by the human FX protein. J Biol Chem 271, 27274-27279.
66. Tusnády, G. E. & Simon, I. (1998). Principles governing amino acid composition of integral membrane proteins: application to topology prediction. J Mol Biol 283, 489-506.
67. Whitfield, C. (2006). Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annu Rev Biochem 75, 39-68.
68. Whitfield, C. & Paiment, A. (2003). Biosynthesis and assembly of group 1 capsular polysaccharides in Escherichia coli and related extracellular polysaccharides in other bacteria. Carbohydr Res 338, 2491-2502.
69. Whitfield, C. & Roberts, I. S. (1999). Structure, assembly and regulation of expression of capsules in Escherichia coli. Mol Microbiol 31, 1307-1319.
70. Wiggins, C. A. & Munro, S. (1998). Activity of the yeast MNN1 α-1,3-mannosyltransferase requires a motif conserved in many other families of glycosyltransferases. Proc Natl Acad Sci U S A 95, 7945-7950.
71. Williams, A. H. & Raetz, C. R. (2007). Structural basis for the acyl chain selectivity and mechanism of UDP-N-acetylglucosamine acyltransferase. Proc Natl Acad Sci U S A 104, 13543-13550.
72. Wu, K. M., Li, L. H., Yan, J. J., Tsao, N., Liao, T. L., Tsai, H. C., Fung, C. P., Chen, H. J., Liu, Y. M. & other authors (2009). Genome sequencing and comparative analysis of Klebsiella pneumoniae NTUH-K2044, a strain causing liver abscess and meningitis. J Bacteriol 191, 4492-4501.
73. Yu, V. L., Hansen, D. S., Ko, W. C., Sagnimeni, A., Klugman, K. P., von Gottberg, A., Goossens, H., Wagener, M. M. & Benedi, V. J. (2007). Virulence characteristics of Klebsiella and clinical manifestations of K. pneumoniae bloodstream infections. Emerg Infect Dis 13, 986-993.