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. 1997 Apr;179(8):2740–2747. doi: 10.1128/jb.179.8.2740-2747.1997

Novel Vibrio cholerae O139 genes involved in lipopolysaccharide biosynthesis.

U H Stroeher 1, G Parasivam 1, B K Dredge 1, P A Manning 1
PMCID: PMC179025  PMID: 9098074

Abstract

The sequence of part of the rfb region of Vibrio cholerae serogroup O139 and the physical map of a 35-kb region of the O139 chromosome have been determined. The O139 rfb region presented contains a number of open reading frames which show similarities to other rfb and capsular biosynthesis genes found in members of the Enterobacteriaceae family and in V. cholerae O1. The cloned and sequenced region can complement the defects in O139 antigen biosynthesis in transposon insertions within the O139 rfb cluster. Linkage is demonstrated among IS1358 of V. cholerae O139, the rfb region, and the recently reported otnA and otnB genes (E. M. Bik, A. E. Bunschoten, R. D. Gouw, and F. R. Mooi, EMBO J. 14:209-216, 1995). In addition, the whole of this region has been linked to the rfaD gene. Furthermore, determination of the sequence flanking IS1358 has revealed homology to other rfb-like genes. The exact site of insertion with respect to rfaD is defined for the novel DNAs of both the Bengal and the Argentinian O139 isolates.

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Selected References

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  1. Bastin D. A., Reeves P. R. Sequence and analysis of the O antigen gene (rfb) cluster of Escherichia coli O111. Gene. 1995 Oct 16;164(1):17–23. doi: 10.1016/0378-1119(95)00459-j. [DOI] [PubMed] [Google Scholar]
  2. Bastin D. A., Romana L. K., Reeves P. R. Molecular cloning and expression in Escherichia coli K-12 of the rfb gene cluster determining the O antigen of an E. coli O111 strain. Mol Microbiol. 1991 Sep;5(9):2223–2231. doi: 10.1111/j.1365-2958.1991.tb02152.x. [DOI] [PubMed] [Google Scholar]
  3. Bhattacharya M. K., Bhattacharya S. K., Garg S., Saha P. K., Dutta D., Nair G. B., Deb B. C., Das K. P. Outbreak of Vibrio cholerae non-O1 in India and Bangladesh. Lancet. 1993 May 22;341(8856):1346–1347. doi: 10.1016/0140-6736(93)90855-b. [DOI] [PubMed] [Google Scholar]
  4. Bik E. M., Bunschoten A. E., Gouw R. D., Mooi F. R. Genesis of the novel epidemic Vibrio cholerae O139 strain: evidence for horizontal transfer of genes involved in polysaccharide synthesis. EMBO J. 1995 Jan 16;14(2):209–216. doi: 10.1002/j.1460-2075.1995.tb06993.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bik E. M., Bunschoten A. E., Willems R. J., Chang A. C., Mooi F. R. Genetic organization and functional analysis of the otn DNA essential for cell-wall polysaccharide synthesis in Vibrio cholerae O139. Mol Microbiol. 1996 May;20(4):799–811. doi: 10.1111/j.1365-2958.1996.tb02518.x. [DOI] [PubMed] [Google Scholar]
  6. Bugert P., Geider K. Molecular analysis of the ams operon required for exopolysaccharide synthesis of Erwinia amylovora. Mol Microbiol. 1995 Mar;15(5):917–933. doi: 10.1111/j.1365-2958.1995.tb02361.x. [DOI] [PubMed] [Google Scholar]
  7. Capage M., Hill C. W. Preferential unequal recombination in the glyS region of the Escherichia coli chromosome. J Mol Biol. 1979 Jan 5;127(1):73–87. doi: 10.1016/0022-2836(79)90460-1. [DOI] [PubMed] [Google Scholar]
  8. Collins L. V., Hackett J. Molecular cloning, characterization, and nucleotide sequence of the rfc gene, which encodes an O-antigen polymerase of Salmonella typhimurium. J Bacteriol. 1991 Apr;173(8):2521–2529. doi: 10.1128/jb.173.8.2521-2529.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Comstock L. E., Johnson J. A., Michalski J. M., Morris J. G., Jr, Kaper J. B. Cloning and sequence of a region encoding a surface polysaccharide of Vibrio cholerae O139 and characterization of the insertion site in the chromosome of Vibrio cholerae O1. Mol Microbiol. 1996 Feb;19(4):815–826. doi: 10.1046/j.1365-2958.1996.407928.x. [DOI] [PubMed] [Google Scholar]
  10. Comstock L. E., Maneval D., Jr, Panigrahi P., Joseph A., Levine M. M., Kaper J. B., Morris J. G., Jr, Johnson J. A. The capsule and O antigen in Vibrio cholerae O139 Bengal are associated with a genetic region not present in Vibrio cholerae O1. Infect Immun. 1995 Jan;63(1):317–323. doi: 10.1128/iai.63.1.317-323.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Davis M. A., Simons R. W., Kleckner N. Tn10 protects itself at two levels from fortuitous activation by external promoters. Cell. 1985 Nov;43(1):379–387. doi: 10.1016/0092-8674(85)90043-1. [DOI] [PubMed] [Google Scholar]
  12. Fallarino A., Mavrangelos C., Stroeher U. H., Manning P. A. Identification of additional genes required for O-antigen biosynthesis in Vibrio cholerae O1. J Bacteriol. 1997 Apr;179(7):2147–2153. doi: 10.1128/jb.179.7.2147-2153.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Goethals K., Mergaert P., Gao M., Geelen D., Van Montagu M., Holsters M. Identification of a new inducible nodulation gene in Azorhizobium caulinodans. Mol Plant Microbe Interact. 1992 Sep-Oct;5(5):405–411. doi: 10.1094/mpmi-5-405. [DOI] [PubMed] [Google Scholar]
  14. Goldman R. C., White D., Orskov F., Orskov I., Rick P. D., Lewis M. S., Bhattacharjee A. K., Leive L. A surface polysaccharide of Escherichia coli O111 contains O-antigen and inhibits agglutination of cells by O-antiserum. J Bacteriol. 1982 Sep;151(3):1210–1221. doi: 10.1128/jb.151.3.1210-1221.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gustafson C. E., Chu S., Trust T. J. Mutagenesis of the paracrystalline surface protein array of Aeromonas salmonicida by endogenous insertion elements. J Mol Biol. 1994 Apr 8;237(4):452–463. doi: 10.1006/jmbi.1994.1247. [DOI] [PubMed] [Google Scholar]
  16. Hill C. W., Sandt C. H., Vlazny D. A. Rhs elements of Escherichia coli: a family of genetic composites each encoding a large mosaic protein. Mol Microbiol. 1994 Jun;12(6):865–871. doi: 10.1111/j.1365-2958.1994.tb01074.x. [DOI] [PubMed] [Google Scholar]
  17. Hisatsune K., Kondo S., Isshiki Y., Iguchi T., Kawamata Y., Shimada T. O-antigenic lipopolysaccharide of Vibrio cholerae O139 Bengal, a new epidemic strain for recent cholera in the Indian subcontinent. Biochem Biophys Res Commun. 1993 Nov 15;196(3):1309–1315. doi: 10.1006/bbrc.1993.2395. [DOI] [PubMed] [Google Scholar]
  18. Hitchcock P. J., Brown T. M. Morphological heterogeneity among Salmonella lipopolysaccharide chemotypes in silver-stained polyacrylamide gels. J Bacteriol. 1983 Apr;154(1):269–277. doi: 10.1128/jb.154.1.269-277.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hobbs M., Reeves P. R. The JUMPstart sequence: a 39 bp element common to several polysaccharide gene clusters. Mol Microbiol. 1994 Jun;12(5):855–856. doi: 10.1111/j.1365-2958.1994.tb01071.x. [DOI] [PubMed] [Google Scholar]
  20. Jiang X. M., Neal B., Santiago F., Lee S. J., Romana L. K., Reeves P. R. Structure and sequence of the rfb (O antigen) gene cluster of Salmonella serovar typhimurium (strain LT2). Mol Microbiol. 1991 Mar;5(3):695–713. doi: 10.1111/j.1365-2958.1991.tb00741.x. [DOI] [PubMed] [Google Scholar]
  21. Johnson J. A., Salles C. A., Panigrahi P., Albert M. J., Wright A. C., Johnson R. J., Morris J. G., Jr Vibrio cholerae O139 synonym bengal is closely related to Vibrio cholerae El Tor but has important differences. Infect Immun. 1994 May;62(5):2108–2110. doi: 10.1128/iai.62.5.2108-2110.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Karaolis D. K., Lan R., Reeves P. R. Molecular evolution of the seventh-pandemic clone of Vibrio cholerae and its relationship to other pandemic and epidemic V. cholerae isolates. J Bacteriol. 1994 Oct;176(20):6199–6206. doi: 10.1128/jb.176.20.6199-6206.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Knirel Y. A., Paredes L., Jansson P. E., Weintraub A., Widmalm G., Albert M. J. Structure of the capsular polysaccharide of Vibrio cholerae O139 synonym Bengal containing D-galactose 4,6-cyclophosphate. Eur J Biochem. 1995 Sep 1;232(2):391–396. doi: 10.1111/j.1432-1033.1995.391zz.x. [DOI] [PubMed] [Google Scholar]
  24. Kyte J., Doolittle R. F. A simple method for displaying the hydropathic character of a protein. J Mol Biol. 1982 May 5;157(1):105–132. doi: 10.1016/0022-2836(82)90515-0. [DOI] [PubMed] [Google Scholar]
  25. Lee S. J., Romana L. K., Reeves P. R. Sequence and structural analysis of the rfb (O antigen) gene cluster from a group C1 Salmonella enterica strain. J Gen Microbiol. 1992 Sep;138(9):1843–1855. doi: 10.1099/00221287-138-9-1843. [DOI] [PubMed] [Google Scholar]
  26. Lindberg B., Lindh F., Lönngren J. Structural studies of the O-specific side-chain of the lipopolysaccharide from Escherichia coli O 55. Carbohydr Res. 1981 Nov 2;97(1):105–112. doi: 10.1016/s0008-6215(00)80528-5. [DOI] [PubMed] [Google Scholar]
  27. Macpherson D. F., Morona R., Beger D. W., Cheah K. C., Manning P. A. Genetic analysis of the rfb region of Shigella flexneri encoding the Y serotype O-antigen specificity. Mol Microbiol. 1991 Jun;5(6):1491–1499. doi: 10.1111/j.1365-2958.1991.tb00795.x. [DOI] [PubMed] [Google Scholar]
  28. Manning P. A., Heuzenroeder M. W., Yeadon J., Leavesley D. I., Reeves P. R., Rowley D. Molecular cloning and expression in Escherichia coli K-12 of the O antigens of the Inaba and Ogawa serotypes of the Vibrio cholerae O1 lipopolysaccharides and their potential for vaccine development. Infect Immun. 1986 Aug;53(2):272–277. doi: 10.1128/iai.53.2.272-277.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Morona R., Brown M. H., Yeadon J., Heuzenroeder M. W., Manning P. A. Effect of lipopolysaccharide core synthesis mutations on the production of Vibrio cholerae O-antigen in Escherichia coli K-12. FEMS Microbiol Lett. 1991 Aug 15;66(3):279–285. doi: 10.1016/0378-1097(91)90274-e. [DOI] [PubMed] [Google Scholar]
  30. Morona R., Mavris M., Fallarino A., Manning P. A. Characterization of the rfc region of Shigella flexneri. J Bacteriol. 1994 Feb;176(3):733–747. doi: 10.1128/jb.176.3.733-747.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Nair G. B., Ramamurthy T., Bhattacharya S. K., Mukhopadhyay A. K., Garg S., Bhattacharya M. K., Takeda T., Shimada T., Takeda Y., Deb B. C. Spread of Vibrio cholerae O139 Bengal in India. J Infect Dis. 1994 May;169(5):1029–1034. doi: 10.1093/infdis/169.5.1029. [DOI] [PubMed] [Google Scholar]
  32. Preston L. M., Xu Q., Johnson J. A., Joseph A., Maneval D. R., Jr, Husain K., Reddy G. P., Bush C. A., Morris J. G., Jr Preliminary structure determination of the capsular polysaccharide of Vibrio cholerae O139 Bengal Al1837. J Bacteriol. 1995 Feb;177(3):835–838. doi: 10.1128/jb.177.3.835-838.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Ramamurthy T., Garg S., Sharma R., Bhattacharya S. K., Nair G. B., Shimada T., Takeda T., Karasawa T., Kurazano H., Pal A. Emergence of novel strain of Vibrio cholerae with epidemic potential in southern and eastern India. Lancet. 1993 Mar 13;341(8846):703–704. doi: 10.1016/0140-6736(93)90480-5. [DOI] [PubMed] [Google Scholar]
  34. Rivas M., Toma C., Miliwebsky E., Caffer M. I., Galas M., Varela P., Tous M., Bru A. M., Binsztein N. Cholera isolates in relation to the "eighth pandemic". Lancet. 1993 Oct 9;342(8876):926–927. [PubMed] [Google Scholar]
  35. Schulz V. P., Reznikoff W. S. Translation initiation of IS50R read-through transcripts. J Mol Biol. 1991 Sep 5;221(1):65–80. doi: 10.1016/0022-2836(91)80205-9. [DOI] [PubMed] [Google Scholar]
  36. Sharma D. P., Stroeher U. H., Thomas C. J., Manning P. A., Attridge S. R. The toxin-coregulated pilus (TCP) of Vibrio cholerae: molecular cloning of genes involved in pilus biosynthesis and evaluation of TCP as a protective antigen in the infant mouse model. Microb Pathog. 1989 Dec;7(6):437–448. doi: 10.1016/0882-4010(89)90024-7. [DOI] [PubMed] [Google Scholar]
  37. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  38. Stroeher U. H., Jedani K. E., Dredge B. K., Morona R., Brown M. H., Karageorgos L. E., Albert M. J., Manning P. A. Genetic rearrangements in the rfb regions of Vibrio cholerae O1 and O139. Proc Natl Acad Sci U S A. 1995 Oct 24;92(22):10374–10378. doi: 10.1073/pnas.92.22.10374. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Stroeher U. H., Karageorgos L. E., Brown M. H., Morona R., Manning P. A. A putative pathway for perosamine biosynthesis is the first function encoded within the rfb region of Vibrio cholerae O1. Gene. 1995 Dec 1;166(1):33–42. doi: 10.1016/0378-1119(95)00589-0. [DOI] [PubMed] [Google Scholar]
  40. Stroeher U. H., Karageorgos L. E., Morona R., Manning P. A. In Vibrio cholerae serogroup O1, rfaD is closely linked to the rfb operon. Gene. 1995 Mar 21;155(1):67–72. doi: 10.1016/0378-1119(94)00923-g. [DOI] [PubMed] [Google Scholar]
  41. Stroeher U. H., Karageorgos L. E., Morona R., Manning P. A. Serotype conversion in Vibrio cholerae O1. Proc Natl Acad Sci U S A. 1992 Apr 1;89(7):2566–2570. doi: 10.1073/pnas.89.7.2566. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Szabo M., Bronner D., Whitfield C. Relationships between rfb gene clusters required for biosynthesis of identical D-galactose-containing O antigens in Klebsiella pneumoniae serotype O1 and Serratia marcescens serotype O16. J Bacteriol. 1995 Mar;177(6):1544–1553. doi: 10.1128/jb.177.6.1544-1553.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Tabor S., Richardson C. C. A bacteriophage T7 RNA polymerase/promoter system for controlled exclusive expression of specific genes. Proc Natl Acad Sci U S A. 1985 Feb;82(4):1074–1078. doi: 10.1073/pnas.82.4.1074. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Taylor R. K., Manoil C., Mekalanos J. J. Broad-host-range vectors for delivery of TnphoA: use in genetic analysis of secreted virulence determinants of Vibrio cholerae. J Bacteriol. 1989 Apr;171(4):1870–1878. doi: 10.1128/jb.171.4.1870-1878.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Thorson J. S., Lo S. F., Ploux O., He X., Liu H. W. Studies of the biosynthesis of 3,6-dideoxyhexoses: molecular cloning and characterization of the asc (ascarylose) region from Yersinia pseudotuberculosis serogroup VA. J Bacteriol. 1994 Sep;176(17):5483–5493. doi: 10.1128/jb.176.17.5483-5493.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Weintraub A., Widmalm G., Jansson P. E., Jansson M., Hultenby K., Albert M. J. Vibrio cholerae O139 Bengal possesses a capsular polysaccharide which may confer increased virulence. Microb Pathog. 1994 Mar;16(3):235–241. doi: 10.1006/mpat.1994.1024. [DOI] [PubMed] [Google Scholar]
  47. Wyk P., Reeves P. Identification and sequence of the gene for abequose synthase, which confers antigenic specificity on group B salmonellae: homology with galactose epimerase. J Bacteriol. 1989 Oct;171(10):5687–5693. doi: 10.1128/jb.171.10.5687-5693.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Xiang S. H., Haase A. M., Reeves P. R. Variation of the rfb gene clusters in Salmonella enterica. J Bacteriol. 1993 Aug;175(15):4877–4884. doi: 10.1128/jb.175.15.4877-4884.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Xiang S. H., Hobbs M., Reeves P. R. 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. 1994 Jul;176(14):4357–4365. doi: 10.1128/jb.176.14.4357-4365.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Zhao S., Sandt C. H., Feulner G., Vlazny D. A., Gray J. A., Hill C. W. Rhs elements of Escherichia coli K-12: complex composites of shared and unique components that have different evolutionary histories. J Bacteriol. 1993 May;175(10):2799–2808. doi: 10.1128/jb.175.10.2799-2808.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]

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