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. 1969 Oct;100(1):433–444. doi: 10.1128/jb.100.1.433-444.1969

Biosynthesis of Cell Wall Lipopolysaccharide in Mutants of Salmonella V. A Mutant of Salmonella typhimurium Defective in the Synthesis of Cytidine Diphosphoabequose

Ryosuke Yuasa a,1, Mark Levinthal b, Hiroshi Nikaido c,2
PMCID: PMC315411  PMID: 4899003

Abstract

A mutant of Salmonella typhimurium LT2 was found to be unable to convert cytidine diphospho-4-keto-6-deoxy-d-glucose into cytidine diphosphoabequose. The mutation maps in the rfb gene cluster, which is known to be involved in the biosynthesis of the peripheral, “O side-chain” portion of cell wall lipopolysaccharide. In spite of the fact that, in the O side chains, abequose is not a part of the main chain but occurs as short branches, the mutant appears to be unable to polymerize oligosaccharide “repeat units” into long O side chains. The following evidence indicates that this failure is the result of the absence of cytidine diphosphoabequose rather than that of a superimposed second mutation in other genes of the rfb cluster. (i) The mutant does not behave like a multisite mutant in genetic crosses, and it gives rise, at a high frequency, to “revertants” where the ability to synthesize cytidine diphosphoabequose and the ability to synthesize normal lipopolysaccharide with O side chains are both restored. (ii) The mutant strain has normal levels of activity of all of the other enzymes known to be involved in O side-chain synthesis, except that the levels of several enzymes were lowered by about 30% owing to the polarity effect of the mutation. That the lowering of these enzymes is not responsible for the failure of the mutant to synthesize O side chains is clear from the fact that there were revertants which had regained some ability to synthesize abequose but still had lowered levels of these other enzymes, and that this type of revertant produced lipopolysaccharide with considerable amounts of O side chains.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. BECKMANN I., SUBBAIAH T. V., STOCKER B. A. ROUGH MUTANTS OF SALMONELLA TYPHIMURIUM. II. SEROLOGICAL AND CHEMICAL INVESTIGATIONS. Nature. 1964 Mar 28;201:1299–1301. doi: 10.1038/2011299a0. [DOI] [PubMed] [Google Scholar]
  2. BERTANI G. Studies on lysogenesis. I. The mode of phage liberation by lysogenic Escherichia coli. J Bacteriol. 1951 Sep;62(3):293–300. doi: 10.1128/jb.62.3.293-300.1951. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Brenner S., Barnett L., Katz E. R., Crick F. H. UGA: a third nonsense triplet in the genetic code. Nature. 1967 Feb 4;213(5075):449–450. doi: 10.1038/213449a0. [DOI] [PubMed] [Google Scholar]
  4. FUKASAWA T., NIKAIDO H. Galactose-sensitive mutants of Salmonella. II. Bacteriolysis induced by galactose. Biochim Biophys Acta. 1961 Apr 15;48:470–483. doi: 10.1016/0006-3002(61)90045-2. [DOI] [PubMed] [Google Scholar]
  5. Gemski P., Jr, Stocker B. A. Transduction by bacteriophage P22 in nonsmooth mutants of Salmonella typhimurium. J Bacteriol. 1967 May;93(5):1588–1597. doi: 10.1128/jb.93.5.1588-1597.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Higashi Y., Strominger J. L., Sweeley C. C. Structure of a lipid intermediate in cell wall peptidoglycan synthesis: a derivative of a C55 isoprenoid alcohol. Proc Natl Acad Sci U S A. 1967 Jun;57(6):1878–1884. doi: 10.1073/pnas.57.6.1878. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Kalckar H. M., Kurahashi K., Jordan E. HEREDITARY DEFECTS IN GALACTOSE METABOLISM IN ESCHERICHIA COLI MUTANTS, I. DETERMINATION OF ENZYME ACTIVITIES. Proc Natl Acad Sci U S A. 1959 Dec;45(12):1776–1786. doi: 10.1073/pnas.45.12.1776. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Kent J. L., Osborn M. J. Properties of the O-specific hapten formed in vivo by mutant strains of Salmonella typhimurium. Biochemistry. 1968 Dec;7(12):4396–4408. doi: 10.1021/bi00852a036. [DOI] [PubMed] [Google Scholar]
  9. Lüderitz O., Staub A. M., Westphal O. Immunochemistry of O and R antigens of Salmonella and related Enterobacteriaceae. Bacteriol Rev. 1966 Mar;30(1):192–255. doi: 10.1128/br.30.1.192-255.1966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. NAIDE Y., NIKAIDO H., MAEKELAE P. H., WILKINSON R. G., STOCKER B. A. SEMIROUGH STRAINS OF SALMONELLA. Proc Natl Acad Sci U S A. 1965 Jan;53:147–153. doi: 10.1073/pnas.53.1.147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. NIKAIDO H., JOKURA K. Isolation of cytidine diphosphate 3,6-dideoxyhexoses from Salmonella. Biochem Biophys Res Commun. 1961 Nov 29;6:304–309. doi: 10.1016/0006-291x(61)90384-9. [DOI] [PubMed] [Google Scholar]
  12. NIKAIDO H., MIKAIDO K., SUBBAIAH T. V., STOCKER B. A. ROUGH MUTANTS OF SALMONELLA TYPHIMURIUM. III. ENZYMATIC SYNTHESIS OF NUCLEOTIDE-SUGAR COMPOUNDS. Nature. 1964 Mar 28;201:1301–1302. doi: 10.1038/2011301a0. [DOI] [PubMed] [Google Scholar]
  13. NIKAIDO H., NIKAIDO K. BIOSYNTHESIS OF CELL WALL POLYSACCHARIDE IN MUTANT STRAINS OF SALMONELLA. IV. SYNTHESIS OF S-SPECIFIC SIDE-CHAIN. Biochem Biophys Res Commun. 1965 Apr 23;19:322–327. doi: 10.1016/0006-291x(65)90462-6. [DOI] [PubMed] [Google Scholar]
  14. Nikaido H. Biosynthesis of cell wall polysaccharide in mutant strains of Salmonella. 3. Transfer of L-rhamnose and D-galactose. Biochemistry. 1965 Aug;4(8):1550–1561. doi: 10.1021/bi00884a014. [DOI] [PubMed] [Google Scholar]
  15. Nikaido H., Levinthal M., Nikaido K., Nakane K. Extended deletions in the histidine-rough-B region of the Salmonella chromosome. Proc Natl Acad Sci U S A. 1967 Jun;57(6):1825–1832. doi: 10.1073/pnas.57.6.1825. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Nikaido H., Nikaido K. Enzymatic synthesis of cytidine diphosphate 3,6-dideoxyhexoses in Salmonella. J Biol Chem. 1966 Mar 25;241(6):1376–1385. [PubMed] [Google Scholar]
  17. Nikaido H., Nikaido K., Mäkelä P. H. Genetic determination of enzymes synthesizing O-specific sugars of Salmonella lipopolysaccharides. J Bacteriol. 1966 Mar;91(3):1126–1135. doi: 10.1128/jb.91.3.1126-1135.1966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Nikaido H. Structure of cell wall lipopolysaccharide from Salmonella typhimurium. I. Linkage between o side chains and R core. J Biol Chem. 1969 Jun 10;244(11):2835–2845. [PubMed] [Google Scholar]
  19. Osborn M. J., Weiner I. M. Biosynthesis of a bacterial lipopolysaccharide. VI. Mechanism of incorporation of abequose into the O-antigen of Salmonella typhimurium. J Biol Chem. 1968 May 25;243(10):2631–2639. [PubMed] [Google Scholar]
  20. Pape H., Strominger J. L. Enzymatic synthesis of cytidine diphosphate 3,6-dideoxyhexoses. V. Partial purification of the two protein components required for introduction of the 3-deoxy group. J Biol Chem. 1969 Jul 10;244(13):3598–3604. [PubMed] [Google Scholar]
  21. STRUVE W. G., NEUHAUS F. C. EVIDENCE FOR AN INITIAL ACCEPTOR OF UDP-NAC-MURAMYL-PENTAPEPTIDE IN THE SYNTHESIS OF BACTERIAL MUCOPEPTIDE. Biochem Biophys Res Commun. 1965 Jan 4;18:6–12. doi: 10.1016/0006-291x(65)90873-9. [DOI] [PubMed] [Google Scholar]
  22. Weiner I. M., Higuchi T., Rothfield L., Saltmarsh-Andrew M., Osborn M. J., Horecker B. L. Biosynthesis of bacterial lipopolysaccharide. V. Lipid-linked intermediates in the biosynthesis of the O-antigen groups of Salmonella typhimurium. Proc Natl Acad Sci U S A. 1965 Jul;54(1):228–235. doi: 10.1073/pnas.54.1.228. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Whitfield H. J., Jr, Martin R. G., Ames B. N. Classification of aminotransferase (C gene) mutants in the histidine operon. J Mol Biol. 1966 Nov 14;21(2):335–355. doi: 10.1016/0022-2836(66)90103-3. [DOI] [PubMed] [Google Scholar]
  24. Wilkinson R. G., Stocker B. A. Genetics and cultural properties of mutants of Salmonella typhimurium lacking glucosyl or galactosyl lipopolysaccharide transferases. Nature. 1968 Mar 9;217(5132):955–957. doi: 10.1038/217955a0. [DOI] [PubMed] [Google Scholar]
  25. Wright A., Dankert M., Fennessey P., Robbins P. W. Characterization of a polyisoprenoid compound functional in O-antigen biosynthesis. Proc Natl Acad Sci U S A. 1967 Jun;57(6):1798–1803. doi: 10.1073/pnas.57.6.1798. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. ZELEZNICK L. D., ROSEN S. M., SALTMARSH-ANDREW M., OSBORN M. J., HORECKER B. L. BIOSYNTHESIS OF BACTERIAL LIPOPOLYSACCHARIDE, IV. ENZYMATIC INCORPORATION OF MANNOSE, RHAMNOSE, AND GALACTOSE IN A MUTANT STRAIN OF SALMONELLA TYPHIMURIUM. Proc Natl Acad Sci U S A. 1965 Jan;53:207–214. doi: 10.1073/pnas.53.1.207. [DOI] [PMC free article] [PubMed] [Google Scholar]

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