Abstract
O antigen is part of the lipopolysaccharide present in the outer membrane of Gram-negative bacteria. It has many different forms, which are almost entirely due to genetic variations of O antigen gene clusters. In this study, the O antigen gene clusters of E. coli O24 and O56 were sequenced, and all genes were assigned functions on the basis of homology. Comparison of O antigen gene clusters indicated that E. coli O24 O antigen gene cluster has possibly arisen from the E. coli O56 gene cluster, through inactivation of two glycosyltransferase genes and acquisition of two new genes from E. coli O157 and O152, respectively. The insertion sequence elements seemed to play important roles for the assembly of the O24 O antigen gene cluster. This is the first time that the evolutionary history of a multi-origin O antigen gene cluster is clearly demonstrated. Genes specific to E. coli O24 and O56 were also identified, which may be used for development of DNA-based serotyping schemes.
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Literature Cited
Samuel G, Reeves P (2003) Biosynthesis of O-antigens: genes and pathways involved in nucleotide sugar precursor synthesis and O-antigen assembly. Carbohydr Res 338:2503–2519
Wang L, Jensen S, Hallman R, Reeves PR (1998) Expression of the O antigen gene cluster is regulated by RfaH through the JUMPstart sequence. FEMS Microbiol Lett 165:201–206
Samuel G, Hogbin JP, Wang L, Reeves PR (2004) Relationships of the Escherichia coli O157, O111, and O55 O-antigen gene clusters with those of Salmonella enterica and Citrobacter freundii, which express identical O antigens. J Bacteriol 186:6536–6543
Nelson K, Selander RK (1994) Intergeneric transfer and recombination of the 6-phosphogluconate dehydrogenase gene (gnd) in enteric bacteria. Proc Natl Acad Sci USA 91:10227–10231
Lai V, Wang L, Reeves PR (1998) Escherichia coli clone Sonnei (Shigella sonnei) had a chromosomal O-antigen gene cluster prior to gaining its current plasmid-borne O-antigen genes. J Bacteriol 180:2983–2986
Xu DQ, Cisar JO, Ambulos NJ, Burr DH, Kopecko DJ (2002) Molecular cloning and characterization of genes for Shigella sonnei form I O polysaccharide: proposed biosynthetic pathway and stable expression in a live Salmonella vaccine vector. Infect Immun 70:4414–4423
Curd H, Liu D, Reeves PR (1998) Relationships among the O-Antigen gene clusters of Salmonella enterica groups B, D1, D2, and D3. J Bacteriol 180:1002–1007
Xiang SH, Hobbs M, Reeves PR (1994) Molecular analysis of the rfb gene cluster of a group D2 Salmonella enterica strain: evidence for its origin from an insertion sequence-mediated recombination event between group E and D1 strains. J Bacteriol 176:4357–4365
Pacinelli E, Wang L, Reeves PR (2002) Relationship of Yersinia pseudotuberculosis O antigens IA, IIA, and IVB: the IIA gene cluster was derived from that of IVB. Infect Immun 70:3271–3276
Gamian A, Kenne L (1993) Analysis of 7-substituted sialic acid in some enterobacterial lipopolysaccharides. J Bacteriol 175:1508–1513
Feng L, Senchenkova SN, Yang J, Shashkov AS, Tao J, Guo H, Zhao G, Knirel YA, Reeves P, Wang L (2004) Structural and genetic characterization of the Shigella boydii Type 13 O antigen. J Bacteriol 182:383–392
Bastin DA, Reeves PR (1995) Sequence and analysis of the O antigen gene (rfb) cluster of Escherichia coli O111. Gene 164:17–23
Wang L, Briggs CE, Rothemund D, Fratamico P, Luchansky JB, Reeves PR (2001) Sequence of the E. coli O104 antigen gene cluster and identification of O104 specific genes. Gene 270:231–236
Wang L, Reeves PR (1998) Organization of Escherichia coli O157 O antigen gene cluster and identification of its specific genes. Infect Immun 66:3545–3551
Staden R (1996) The Staden Sequence Analysis Package. Mol Biotech 5:233–241
Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, Rajandream MA, Barrell B (2000) Artemis: sequence visualisation and annotation. Bioinformatics 16:944–945
Wernersson R, Pedersen AG (2003) RevTrans: Multiple alignment of coding DNA from aligned amino acid sequences. Nucleic Acids Res 31:3537–3539
Comeron JM (1999) K-Estimator: Calculation of the number of nucleotide substitutions per site and the confidence intervals. Bioinformatics 15:763–764
Datsenko KA, Wanner BL (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97:6640–6645
Wang L, Huskic S, Cisterne A, Rothemund D, Reeves PR (2002) The O-antigen gene cluster of Escherichia coli O55:H7 and identification of a new UDP-GlcNAc C4 epimerase gene. J Bacteriol 184:2620–2625
Wang L, Reeves PR (1994) Involvement of the galactosyl-1-phosphate transferase encoded by the Salmonella enterica rfbP gene in O antigen subunit processing. J Bacteriol 176:4348–4356
Wang L, Curd H, Qu W, Reeves PR (1998) Sequencing of Escherichia coli O111 O-antigen gene cluster and identification of O111-specific genes. J Clin Microbiol 36:3182–3187
Reeves PR, Wang L (2002) Genomic organization of LPS-specific loci. Curr Top Microbiol Immunol 264:109–135
Daines DA, Wright LF, Chaffin DO, Rubens CE, Silver RP (2000) NeuD plays a role in the synthesis of sialic acid in Escherichia coli K1. FEMS Microbiol Lett 189:281–284
Amer AO, Valvano MA (2000) The N-terminal region of the Escherichia coli WecA (Rfe) protein, containing three predicted transmembrane helices, is required for function but not for membrane insertion. J Bacteriol 182:498–503
Jones PA, Samuels NM, Phillips NJ, Munson RJ, Bozue JA, Arseneau JA, Nichols WA, Zaleski A, Gibson BW, Apicella MA (2002) Haemophilus influenzae type b strain A2 has multiple sialyltransferases involved in lipooligosaccharide sialylation. J Biol Chem 277:14598–14611
Olsson U, Lycknert K, Stenutz R, Weintraub A, Widmalm G (2005) Structural analysis of the O-antigen polysaccharide from Escherichia coli O152. Carbohydr Res 340:167–171
Morona R, Mavris M, Fallarino A, Manning PA (1994) Characterisation of the ssrfc region of Shigella flexneri. J Bacteriol 176:733–747
Torgov VI, Shashkov AS, Jann B, Jann K (1995) NMR reinvestigation of two N-acetylneuraminic acid-containing O-specific polysaccharides (O56 and O24) of Escherichia coli. Carbohydr Res 272:73–90
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This work was supported by NSFC General Programs (30270029 and 30530010) to L.W. and L.F.
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Cheng, J., Wang, Q., Wang, W. et al. Characterization of E. coli O24 and O56 O Antigen Gene Clusters Reveals a Complex Evolutionary History of the O24 Gene Cluster. Curr Microbiol 53, 470–476 (2006). https://doi.org/10.1007/s00284-006-0032-7
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DOI: https://doi.org/10.1007/s00284-006-0032-7