1887

Abstract

The formation of cyclopropane fatty acid (CFA) and its role in the acid shock response in serovar Typhimurium () was investigated. Data obtained by GC/MS demonstrated that the CFA level in increased upon its entry to the stationary phase, as in other bacteria. The gene encoding CFA synthase was cloned, and mutants of the gene were constructed by allelic exchange. A mutant could not produce CFA and was sensitive to low pH. Introduction of a functional gene into a mutant cell made the mutant convert all unsaturated fatty acids to CFAs and partially restored resistance to low pH. Interestingly, the alternative sigma factor RpoS, which was induced during the stationary phase, affected the production of C CFA but not C CFA. Western blotting analysis showed that the increase in expression of CFA synthase at early stationary phase was due to the alternative sigma factor RpoS.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.27265-0
2005-01-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/151/1/mic1510209.html?itemId=/content/journal/micro/10.1099/mic.0.27265-0&mimeType=html&fmt=ahah

References

  1. Bang I. S., Kim B. H., Foster J. W., Park Y. K. 2000; OmpR regulates the stationary-phase acid tolerance response of Salmonella enterica serovar Typhimurium. J Bacteriol 182:2245–2252 [CrossRef]
    [Google Scholar]
  2. Brown J. L., Ross T., McMeekin T. A., Nichols P. D. 1997; Acid habituation of Escherichia coli and the potential role of cyclopropane fatty acids in low pH tolerance. Int J Food Microbiol 37:163–173 [CrossRef]
    [Google Scholar]
  3. Bullas L. R., Ryu J. I. 1983; Salmonella typhimurium LT2 strains which are r m+ for all three chromosomally located systems for DNA restriction and modification. J Bacteriol 156:471–474
    [Google Scholar]
  4. Chang A. C., Cohen S. N. 1978; Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid. J Bacteriol 134:1141–1156
    [Google Scholar]
  5. Chang Y. Y., Cronan J. E. Jr 1999; Membrane cyclopropane fatty acid content is a major factor in acid resistance of Escherichia coli . Mol Microbiol 33:249–259 [CrossRef]
    [Google Scholar]
  6. Chang Y. Y., Eichel J., Cronan J. E. Jr 2000; Metabolic instability of Escherichia coli cyclopropane fatty acid synthase is due to RpoH-dependent proteolysis. J Bacteriol 182:4288–4294 [CrossRef]
    [Google Scholar]
  7. Cronan J. E. Jr 1968; Phospholipid alterations during growth of Escherichia coli . J Bacteriol 95:2054–2061
    [Google Scholar]
  8. Cronan J. E. Jr, Reed R., Taylor F. R., Jackson M. B. 1979; Properties and biosynthesis of cyclopropane fatty acids in Escherichia coli . J Bacteriol 138:118–121
    [Google Scholar]
  9. Curtiss R. III, Porter S. B., Munson M., Tinge S. A., Hassan J. O., Gentry-Weeks C., Kelly S. M. 1991; Nonrecombinant and recombinant avirulent Salmonella vaccines for poultry. In Colonization Control of Human Bacterial Enteropathogens in Poultry pp 169–198 Edited by Blankenship L. C., Bailey J. H. S., Cox N. A., Stern N. J., Meinersmann R. J. New York, NY: Academic Press;
    [Google Scholar]
  10. de Jonge R., Ritmeester W. S., van Leusden F. M. 2003; Adaptive responses of Salmonella enterica serovar Typhimurium DT104 and other S. Typhimurium strains and Escherichia coli O157 to low pH environments. J Appl Microbiol 94:625–632 [CrossRef]
    [Google Scholar]
  11. Edwards R. A., Keller L. H., Schifferli D. M. 1998; Improved allelic exchange vectors and their use to analyze 987P fimbria gene expression. Gene 207:149–157 [CrossRef]
    [Google Scholar]
  12. Eichel J., Chang Y. Y., Riesenberg D., Cronan J. E. Jr 1999; Effect of ppGpp on Escherichia coli cyclopropane fatty acid synthesis is mediated through the RpoS sigma factor (sigmaS. J Bacteriol 181:572–576
    [Google Scholar]
  13. Foster J. W. 1999; When protons attack; microbial strategies of acid adaptation. Curr Opin Microbiol 2:170–174 [CrossRef]
    [Google Scholar]
  14. Foster J. W., Moreno M. 1999; Inducible acid tolerance mechanisms in enteric bacteria. In Bacterial Response to pH pp 55–70 Edited by Chadwick D. J., Cardew G. Chichester: Wiley;
    [Google Scholar]
  15. Fu R., Voordouw G. 1997; Targeted gene-replacement mutagenesis of dcrA , encoding an oxygen sensor of the sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough. Microbiology 143:1815–1826 [CrossRef]
    [Google Scholar]
  16. Goldfine H. 1972; Comparative aspects of bacterial lipids. Adv Microb Physiol 8:1–58
    [Google Scholar]
  17. Grogan D. W., Cronan J. E. Jr 1984; Cloning and manipulation of the Escherichia coli cyclopropane fatty acid synthase gene: physiological aspects of enzyme overproduction. J Bacteriol 158:286–295
    [Google Scholar]
  18. Grogan D. W., Cronan J. E. Jr 1986; Characterization of Escherichia coli mutants completely defective in synthesis of cyclopropane fatty acids. J Bacteriol 166:872–877
    [Google Scholar]
  19. Grogan D. W., Cronan J. E. Jr 1997; Cyclopropane ring formation in membrane lipids of bacteria. Microbiol Mol Biol Rev 61:429–441
    [Google Scholar]
  20. Guan K. L., Dixon J. E. 1991; Eukaryotic proteins expressed in Escherichia coli : an improved thrombin cleavage and purification procedure of fusion proteins with glutathione S -transferase. Anal Biochem 192:262–267 [CrossRef]
    [Google Scholar]
  21. Haque M., Hirai Y., Yokota K. 7 other authors 1996; Lipid profile of Helicobacter spp.: presence of cholesteryl glucoside as a characteristic feature. J Bacteriol 178:2065–2070
    [Google Scholar]
  22. Haydock S. F., Dowson J. A., Dhillon N., Roberts G. A., Cortes J., Leadlay P. F. 1991; Cloning and sequence analysis of genes involved in erythromycin biosynthesis in Saccharopolyspora erythraea : sequence similarities between EryG and a family of S -adenosylmethionine-dependent methyltransferases. Mol Gen Genet 230:120–128 [CrossRef]
    [Google Scholar]
  23. Huang C. C., Smith C. V., Glickman M. S., Jacobs W. R. Jr, Sacchettini J. C. 2002; Crystal structures of mycolic acid cyclopropane synthases from Mycobacterium tuberculosis . J Biol Chem 277:11559–11569 [CrossRef]
    [Google Scholar]
  24. Ingrosso D. A., Fowler V., Bleibaum J., Clarke S. 1989; Sequence of the d-aspartyl/l-isoaspartyl protein methyltransferase from human erythrocytes. Common sequence motifs for protein, DNA, RNA, and small molecule S -adenosylmethionine-dependent methyltransferases. J Biol Chem 264:20131–20139
    [Google Scholar]
  25. Ivanova A., Renshaw M., Guntaka R. V., Eisenstark A. 1992; DNA base sequence variability in katF (putative sigma factor) gene of Escherichia coli . Nucleic Acids Res 20:5479–5480 [CrossRef]
    [Google Scholar]
  26. Jungkind D. L., Wood R. C. 1974; Physiological differences between cyclopropane fatty acid-deficient mutants and the parent strain of Streptococcus faecalis . Biochim Biophys Acta 337:298–310 [CrossRef]
    [Google Scholar]
  27. Law J. H. 1971; Biosynthesis of cyclopropane rings. Acc Chem Res 4:199–203 [CrossRef]
    [Google Scholar]
  28. Lechivalier M. P. 1977; Lipids in bacterial taxonomy – a taxonomist's view. Crit Rev Microbiol 5:109–210 [CrossRef]
    [Google Scholar]
  29. Lee I. S., Slonczewski J. L., Foster J. W. 1994; A low-pH-inducible, stationary-phase acid tolerance response in Salmonella typhimurium . J Bacteriol 176:1422–1426
    [Google Scholar]
  30. Lee I. S., Lin J., Hall H. K., Bearson B., Foster J. W. 1995; The stationary-phase sigma factor sigma S (RpoS) is required for a sustained acid tolerance response in virulent Salmonella typhimurium . Mol Microbiol 17:155–167 [CrossRef]
    [Google Scholar]
  31. Maloy S. R. 1990 Experimental Techniques in Bacterial Genetics Boston, MA: Jones & Bartlett;
    [Google Scholar]
  32. McClelland M., Sanderson K. E., Spieth J. 23 other authors 2001; Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 413:852–856 [CrossRef]
    [Google Scholar]
  33. Moss C. W., Dees S. B. 1975; Identification of microorganisms by gas chromatographic-mass spectrometric analysis of cellular fatty acids. J Chromatogr 112:594–604
    [Google Scholar]
  34. Saha M., Chakraborty A. K. 1992; Studies on phospholipids of different mutants of Salmonella minnesota . Indian J Biochem Biophys 29:355–359
    [Google Scholar]
  35. 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]
  36. Small P., Blankenhorn D., Welty D., Zinser E., Slonczewski J. L. 1994; Acid and base resistance in Escherichia coli and Shigella flexneri : role of rpoS and growth pH. J Bacteriol 176:1729–1737
    [Google Scholar]
  37. Taylor F. R., Cronan J. E. Jr 1976; Selection and properties of Escherichia coli mutants defective in the synthesis of cyclopropane fatty acids. J Bacteriol 125:518–523
    [Google Scholar]
  38. Taylor F. R., Cronan J. E. Jr 1979; Cyclopropane fatty acid synthase of Escherichia coli . Stabilization, purification, and interaction with phospholipid vesicles. Biochemistry 18:3292–3300 [CrossRef]
    [Google Scholar]
  39. Vogel H. J., Bonner D. M. 1956; Acetylornithase of Escherichia coli : partial purification and some properties. J Biol Chem 218:97–106
    [Google Scholar]
  40. Wang A. Y., Cronan J. E. Jr 1994; The growth phase-dependent synthesis of cyclopropane fatty acids in Escherichia coli is the result of an RpoS (KatF)-dependent promoter plus enzyme instability. Mol Microbiol 11:1009–1017 [CrossRef]
    [Google Scholar]
  41. Wang A. Y., Grogan D. W., Cronan J. E. Jr 1992; Cyclopropane fatty acid synthase of Escherichia coli : deduced amino acid sequence, purification, and studies of the enzyme active site. Biochemistry 31:11020–11028 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.27265-0
Loading
/content/journal/micro/10.1099/mic.0.27265-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error