1887

Abstract

No one has, as yet, addressed the relationship between the nature of the outer membrane and cell division. encodes 3-deoxy-D-manno-octulosonic acid (KDO) 8-phosphate synthetase which catalyses the first step in the synthesis of KDO, the linker between lipid A and oligosaccharide of lipopolysaccharide (LPS). Seven temperature-sensitive mutants containing missense mutations in were affected in the production of KDO and all mutants stopped dividing at 41 °C and formed filaments with either one or no FtsZ ring. All observed defects were reversed by the plasmid-borne wild-type gene. Western blotting analysis, however, demonstrated that the amount of FtsZ protein was not affected by the mutation. The mutants were more susceptible to various hydrophobic materials, such as novobiocin, eosin Y and SDS at 36 °C. Methylene blue, however, restored mutant growth. Plasmid-borne wild-type , encoding a lipid A transporter in the ABC family, partially suppressed mutation. A mutation of , functioning at the first stage in lipid A biosynthesis, inhibited both cell division and growth, producing short filaments. These results indicate that the instability of the outer membrane, caused by the defect in KDO biosynthesis, affects FtsZ-ring formation.

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2002-01-01
2024-03-28
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References

  1. Addinall S. G., Bi E., Lutkenhaus J. 1996; FtsZ ring formation in fts mutants. J Bacteriol 178:3877–3884
    [Google Scholar]
  2. Bi E. F., Lutkenhaus J. 1991; FtsZ ring structure associated with division in Escherichia coli . Nature 354:161–164 [CrossRef]
    [Google Scholar]
  3. Buxton R. S., Holland I. B. 1973; Genetic studies of tolerance to colicine E2 in Escherichia coli K-12. I. Relocation and dominance relationships of cet mutations. Mol Gen Genet 127:69–88 [CrossRef]
    [Google Scholar]
  4. Clarke L., Carbon J. 1976; A colony bank containing synthetic ColE1 hybrid plasmids representative of entire E. coli genome. Cell 9:91–99 [CrossRef]
    [Google Scholar]
  5. Clementz T., Bednarski J., Raetz C. R. H. 1996; Function of the htrB high temperature requirement gene of Escherichia coli in the acylation of lipid A. J Biol Chem 271:12095–12102 [CrossRef]
    [Google Scholar]
  6. Dai K., Lutkenhaus J. 1991; FtsZ is an essential cell division gene in Escherichia coli . J Bacteriol 173:3500–3506
    [Google Scholar]
  7. Drlica K. 1984; Biology of bacterial deoxyribonucleic acid topoisomerases. Microbiol Rev 48:273–289
    [Google Scholar]
  8. Hancock R. E. W., Reeves P. 1976; Lipopolysaccharide-deficient, bacteriophage-resistant mutants of Escherichia coli K-12. J Bacteriol 127:98–108
    [Google Scholar]
  9. Hiraga S., Niki H., Ogura T., Ichinose C., Mori H., Ezaki B., Jaffé A. 1989; Chromosome partitioning in Escherichia coli : novel mutants producing anucleate cells. J Bacteriol 171:1496–1505
    [Google Scholar]
  10. Hiraga S., Ichinose C., Niki H., Yamazoe M. 1998; Cell cycle-dependent duplication and bidirectional migration of SeqA-associated DNA–protein complexes in E. coli . Mol Cell 1:381–387 [CrossRef]
    [Google Scholar]
  11. Karkhanis Y. D., Zeltner J. Y., Jackson J. J., Carlo D. J. 1978; A new and improved microassay to determine 2-keto-3-deoxyoctonate in lipopolysaccharide of gram negative bacteria. Anal Biochem 85:595–601 [CrossRef]
    [Google Scholar]
  12. Karow M., Georgopoulos C. 1993; The essential Escherichia coli msbA gene, a multicopy suppressor of null mutations in the htrB gene, is related to the universally conserved family of ATP-dependent translocators. Mol Microbiol 7:69–79 [CrossRef]
    [Google Scholar]
  13. Lehmann V., Rupprecht E., Osborn M. J. 1977; Isolation of mutants conditionally blocked in the biosynthesis of 3-deoxy-d-manno-octulosonic acid-lipid A part of lipopolysaccharides derived from Salmonella typhimurium . Eur J Biochem 76:41–49 [CrossRef]
    [Google Scholar]
  14. Leive L. 1974; The barrier function of the gram negative envelope. Ann NY Acad Sci 235:109–129 [CrossRef]
    [Google Scholar]
  15. Nagai K., Tamura G. 1972; Mutant of Escherichia coli with thermosensitive protein in the process of cellular division. J Bacteriol 112:959–966
    [Google Scholar]
  16. Nikaido H., Vaara M. 1985; Molecular basis of bacterial outer membrane permeability. Microbiol Rev 49:1–32
    [Google Scholar]
  17. Nishimura A., Akiyama K., Kohara Y., Takeda Y., Nishimura Y., Higashitani A., Yasuda S., Horiuchi K., Hirota Y. 1991; Mapping of a whole set of cell division genes in Escherichia coli K-12. In Control of Cell Growth and Division pp 205–223 Edited by Ishihama A. Yoshikawa H. Tokyo: Japan Science Society Press/Berlin: Springer;
    [Google Scholar]
  18. Nishimura A., Akiyama K., Kohara Y., Horiuchi K. 1992; Correlation of a subset of the pLC plasmids to the physical map of Escherichia coli K-12. Microbiol Rev 56:137–151
    [Google Scholar]
  19. Norris V. 1989; Phospholipid flip-out controls the cell cycle of Escherichia coli . J Theor Biol 139:117–128 [CrossRef]
    [Google Scholar]
  20. Osborn M. J., Rick P. D., Rasmussen N. S. 1980; Mechanism of assembly of the outer membrane of Salmonella typhimurium . Translocation and integration of an incomplete mutant lipid A into the outer membrane. J Biol Chem 255:4246–4251
    [Google Scholar]
  21. Radaev S., Dastidar P., Patel M., Woodard R. W., Gatti D. L. 2000; Structure and mechanism of 3-deoxy-d-manno-octulosonate 8-phosphate synthase. J Biol Chem 275:9476–9484 [CrossRef]
    [Google Scholar]
  22. Raetz C. R. H. 1986; Molecular genetics of membrane phospholipid synthesis. Annu Rev Genet 20:253–295 [CrossRef]
    [Google Scholar]
  23. Raetz C. R. H., Purcell S., Meyer M. V., Qureshi N., Takayama K. 1985; Isolation and characterization of eight lipid A precursors from a 3-deoxy-d-manno-octulosonic acid-deficient mutant of Salmonella typhimurium . J Biol Chem 260:16080–16088
    [Google Scholar]
  24. Ray P. H. 1980; Purification and characterization of 3-deoxy-d-manno-octulosonate-8-phosphate synthetase from Escherichia coli . J Bacteriol 141:635–644
    [Google Scholar]
  25. Reeves J. D., Groves D., Clark D. J. 1970; Regulation of cell division in Escherichia coli : characterization of temperature-sensitive division mutants. J Bacteriol 104:1052–1064
    [Google Scholar]
  26. Ricard M., Hirota Y. 1973; Effect osmotique sur le phénotype de mutants thermosensibles d’ E. coli . Ann Inst Pasteur 124:29–43
    [Google Scholar]
  27. Rick P. D., Osborn M. J. 1977; Lipid A mutants of Salmonella typhimurium . Characterization of conditional lethal mutant in 3-deoxy-d-manno-octulosonate-8-phosphate synthetase. J Biol Chem 252:4895–4903
    [Google Scholar]
  28. Rick P. D., Young D. A. 1982; Isolation and characterization of a temperature-sensitive lethal mutant of Salmonella typhimurium that is conditionally defective in 3-deoxy-d-manno-octulosonate-8-phosphate synthetase. J Bacteriol 150:447–455
    [Google Scholar]
  29. Rick P. D., Fung L. W. M., Osborn M. J. 1977; Lipid A mutants of Salmonella typhimurium . Purification and characterization of a lipid A precursor produced by a mutant in 3-deoxy-d-manno-octulosonate-8-phosphate synthetase. J Biol Chem 252:4904–4912
    [Google Scholar]
  30. Rick P. D., Neumeyer B. A., Young D. A. 1983; Effect of altered lipidA synthesis on the synthesis of the OmpA protein in Salmonella typhimurium . J Biol Chem 258:629–635
    [Google Scholar]
  31. Rick P. D., Neumeyer B. A., Young D. A. 1984; Effect of altered lipid A synthesis on the synthesis of major proteins of the Salmonella typhimurium outer membrane. Rev Infect Dis 6:455–462 [CrossRef]
    [Google Scholar]
  32. Rietschel E. T. editor 1984; Chemistry of endotoxin. Handbook of Endotoxin Vol. 1 Amsterdam: Elsevier;
    [Google Scholar]
  33. Sambrook J., Fritsch E. F., Maniatis T. 1989 Molecular Cloning: a Laboratory Manual , 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  34. Sekimizu K. 1994; Interactions between DNA replication-related proteins and phospholipid vesicles in vitro . Chem Phys Lipids 73:223–230 [CrossRef]
    [Google Scholar]
  35. Smit J., Kamio Y., Nikaido H. 1975; Outer membrane of Salmonella typhimurium : chemical analysis and freeze-fracture studies with lipopolysaccharide mutants. J Bacteriol 124:942–958
    [Google Scholar]
  36. Strohmaier H., Remler P., Renner W., Högenauer G. 1995; Expression of genes kdsA and kdsB involved in 3-deoxy-d-manno-octulosonic acid metabolism and biosynthesis of enterobacterial lipopolysaccharide is growth phase regulated primarily at the transcriptional level in Escherichia coli K-12. J Bacteriol 177:4488–4500
    [Google Scholar]
  37. Sun Q., Yu X. C., Margolin W. 1998; Assembly of the FtsZ ring at the central division site in the absence of the chromosome. Mol Microbiol 29:491–503 [CrossRef]
    [Google Scholar]
  38. Tilcock C. P. S. 1986; Lipid polymorphism. Chem Phys Lipids 40:109–125 [CrossRef]
    [Google Scholar]
  39. Wilson G. G., Young K. K. Y., Edlin G. J. 1979; High-frequency generalized transduction by bacteriophage T4. Nature 280:80–82 [CrossRef]
    [Google Scholar]
  40. Woisetschläger M., Högenauer G. 1987; The kdsA gene for 3-deoxy-d-manno-octulosonate-8-phosphate synthetase is part of an operon in Escherichia coli . Mol Gen Genet 207:369–373 [CrossRef]
    [Google Scholar]
  41. Zhou Z., White K. A., Polissi A., Georgopoulos C., Raetz C. R. H. 1998; Function of Escherichia coli MsbA, an essential ABC family transporter, in lipid A and phospholipid biosynthesis. J Biol Chem 273:12466–12475 [CrossRef]
    [Google Scholar]
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