1887

Abstract

The genes are essential for maintaining the outer membrane integrity and detergent resistance in various Gram-negative bacteria, including . The role of TolA has been well established for the bile resistance of subsp. serovar Typhimurium. We compared the bile resistance pattern between the serovars Typhi and Typhimurium and observed that Typhi is more resistant to bile-mediated damage. A closer look revealed a significant difference in the TolA sequence between the two serovars which contributes to the differential detergent resistance. The knockout of both the serovars behaves completely differently in terms of membrane organization and morphology. The role of the Pal proteins and difference in LPS organization between the two serovars were verified and were found to have no direct connection with the altered bile resistance. In normal Luria broth (LB), Typhi Δ is filamentous while Typhimurium Δ grows as single cells, similar to the wild-type. In low osmolarity LB, however, Typhimurium Δ started chaining and Typhi Δ showed no growth. Further investigation revealed that the chaining phenomenon observed was the result of failure of the outer membrane to separate in the dividing cells. Taken together, the results substantiate the evolution of a shorter TolA in Typhi to counteract high bile concentrations, at the cost of lower osmotic tolerance.

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2011-05-01
2019-12-07
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References

  1. Addinall S. G. , Holland B. . ( 2002; ). The tubulin ancestor, FtsZ, draughtsman, designer and driving force for bacterial cytokinesis. . J Mol Biol 318:, 219–236 [CrossRef] [PubMed].
    [Google Scholar]
  2. Baquero M. R. , Bouzon M. , Quintela J. C. , Ayala J. A. , Moreno F. . ( 1996; ). dacD, an Escherichia coli gene encoding a novel penicillin-binding protein (PBP6b) with dd-carboxypeptidase activity. . J Bacteriol 178:, 7106–7111.[PubMed]
    [Google Scholar]
  3. Bernadac A. , Gavioli M. , Lazzaroni J. C. , Raina S. , Lloubès R. . ( 1998; ). Escherichia coli tol-pal mutants form outer membrane vesicles. . J Bacteriol 180:, 4872–4878.[PubMed]
    [Google Scholar]
  4. Bos M. P. , Tommassen J. . ( 2004; ). Biogenesis of the Gram-negative bacterial outer membrane. . Curr Opin Microbiol 7:, 610–616. [CrossRef] [PubMed].
    [Google Scholar]
  5. Bouveret E. , Derouiche R. , Rigal A. , Lloubès R. , Lazdunski C. , Bénédetti H. . ( 1995; ). Peptidoglycan-associated lipoprotein-TolB interaction. A possible key to explaining the formation of contact sites between the inner and outer membranes of Escherichia coli . . J Biol Chem 270:, 11071–11077. [CrossRef] [PubMed]
    [Google Scholar]
  6. Braun V. . ( 1975; ). Covalent lipoprotein from the outer membrane of Escherichia coli . . Biochim Biophys Acta 415:, 335–377.[PubMed] [CrossRef]
    [Google Scholar]
  7. Cascales E. , Bernadac A. , Gavioli M. , Lazzaroni J. C. , Lloubes R. . ( 2002; ). Pal lipoprotein of Escherichia coli plays a major role in outer membrane integrity. . J Bacteriol 184:, 754–759. [CrossRef] [PubMed]
    [Google Scholar]
  8. Clavel T. , Germon P. , Vianney A. , Portalier R. , Lazzaroni J. C. . ( 1998; ). TolB protein of Escherichia coli K-12 interacts with the outer membrane peptidoglycan-associated proteins Pal, Lpp and OmpA. . Mol Microbiol 29:, 359–367. [CrossRef] [PubMed]
    [Google Scholar]
  9. Datsenko K. A. , Wanner B. L. . ( 2000; ). One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. . Proc Natl Acad Sci U S A 97:, 6640–6645. [CrossRef] [PubMed]
    [Google Scholar]
  10. Derouiche R. , Bénédetti H. , Lazzaroni J. C. , Lazdunski C. , Lloubès R. . ( 1995; ). Protein complex within Escherichia coli inner membrane. TolA N-terminal domain interacts with TolQ and TolR proteins. . J Biol Chem 270:, 11078–11084. [CrossRef] [PubMed]
    [Google Scholar]
  11. Dubuisson J. F. , Vianney A. , Hugouvieux-Cotte-Pattat N. , Lazzaroni J. C. . ( 2005; ). Tol-Pal proteins are critical cell envelope components of Erwinia chrysanthemi affecting cell morphology and virulence. . Microbiology 151:, 3337–3347. [CrossRef] [PubMed]
    [Google Scholar]
  12. Gerding M. A. , Ogata Y. , Pecora N. D. , Niki H. , de Boer P. A. . ( 2007; ). The trans-envelope Tol-Pal complex is part of the cell division machinery and required for proper outer-membrane invagination during cell constriction in E. coli . . Mol Microbiol 63:, 1008–1025. [CrossRef] [PubMed]
    [Google Scholar]
  13. Godlewska R. , Wiśniewska K. , Pietras Z. , Jagusztyn-Krynicka E. K. . ( 2009; ). Peptidoglycan-associated lipoprotein (Pal) of Gram-negative bacteria: function, structure, role in pathogenesis and potential application in immunoprophylaxis. . FEMS Microbiol Lett 298:, 1–11. [CrossRef] [PubMed]
    [Google Scholar]
  14. Gunn J. S. . ( 2000; ). Mechanisms of bacterial resistance and response to bile. . Microbes Infect 2:, 907–913. [CrossRef] [PubMed]
    [Google Scholar]
  15. Heidrich C. , Templin M. F. , Ursinus A. , Merdanovic M. , Berger J. , Schwarz H. , de Pedro M. A. , Höltje J. V. . ( 2001; ). Involvement of N-acetylmuramyl-l-alanine amidases in cell separation and antibiotic-induced autolysis of Escherichia coli . . Mol Microbiol 41:, 167–178. [CrossRef] [PubMed]
    [Google Scholar]
  16. Heidrich C. , Ursinus A. , Berger J. , Schwarz H. , Höltje J. V. . ( 2002; ). Effects of multiple deletions of murein hydrolases on viability, septum cleavage, and sensitivity to large toxic molecules in Escherichia coli . . J Bacteriol 184:, 6093–6099. [CrossRef] [PubMed]
    [Google Scholar]
  17. Henderson T. A. , Templin M. , Young K. D. . ( 1995; ). Identification and cloning of the gene encoding penicillin-binding protein 7 of Escherichia coli . . J Bacteriol 177:, 2074–2079.[PubMed]
    [Google Scholar]
  18. Hiemstra H. , Nanninga N. , Woldringh C. L. , Inouye M. , Witholt B. . ( 1987; ). Distribution of newly synthesized lipoprotein over the outer membrane and the peptidoglycan sacculus of an Escherichia coli lac-lpp strain. . J Bacteriol 169:, 5434–5444.[PubMed]
    [Google Scholar]
  19. Holt K. E. , Thomson N. R. , Wain J. , Langridge G. C. , Hasan R. , Bhutta Z. A. , Quail M. A. , Norbertczak H. , Walker D. et al. ( 2009; ). Pseudogene accumulation in the evolutionary histories of Salmonella enterica serovars Paratyphi A and Typhi. . BMC Genomics 10:, 36. [CrossRef] [PubMed]
    [Google Scholar]
  20. Hölzer S. U. , Schlumberger M. C. , Jäckel D. , Hensel M. . ( 2009; ). Effect of the O-antigen length of lipopolysaccharide on the functions of Type III secretion systems in Salmonella enterica . . Infect Immun 77:, 5458–5470. [CrossRef] [PubMed]
    [Google Scholar]
  21. Lahiri A. , Das P. , Chakravortty D. . ( 2009; ). Salmonella Typhimurium: insight into the multi-faceted role of the LysR-type transcriptional regulators in Salmonella . . Int J Biochem Cell Biol 41:, 2129–2133. [CrossRef] [PubMed]
    [Google Scholar]
  22. Lahiri A. , Lahiri A. , Iyer N. , Das P. , Chakravortty D. . ( 2010; ). Visiting the cell biology of Salmonella infection. . Microbes Infect 12:, 809–818. [CrossRef] [PubMed]
    [Google Scholar]
  23. Lazzaroni J. C. , Portalier R. C. . ( 1981; ). Genetic and biochemical characterization of periplasmic-leaky mutants of Escherichia coli K-12. . J Bacteriol 145:, 1351–1358.[PubMed]
    [Google Scholar]
  24. Levengood S. K. , Beyer W. F. Jr , Webster R. E. . ( 1991; ). TolA: a membrane protein involved in colicin uptake contains an extended helical region. . Proc Natl Acad Sci U S A 88:, 5939–5943. [CrossRef] [PubMed]
    [Google Scholar]
  25. Magnet S. , Dubost L. , Marie A. , Arthur M. , Gutmann L. . ( 2008; ). Identification of the l,d-transpeptidases for peptidoglycan cross-linking in Escherichia coli . . J Bacteriol 190:, 4782–4785. [CrossRef] [PubMed]
    [Google Scholar]
  26. Meury J. , Devilliers G. . ( 1999; ). Impairment of cell division in tolA mutants of Escherichia coli at low and high medium osmolarities. . Biol Cell 91:, 67–75. [CrossRef] [PubMed]
    [Google Scholar]
  27. Murray G. L. , Attridge S. R. , Morona R. . ( 2003; ). Regulation of Salmonella typhimurium lipopolysaccharide O antigen chain length is required for virulence; identification of FepE as a second Wzz. . Mol Microbiol 47:, 1395–1406. [CrossRef] [PubMed]
    [Google Scholar]
  28. Paterson G. K. , Northen H. , Cone D. B. , Willers C. , Peters S. E. , Maskell D. J. . ( 2009; ). Deletion of tolA in Salmonella Typhimurium generates an attenuated strain with vaccine potential. . Microbiology 155:, 220–228. [CrossRef] [PubMed]
    [Google Scholar]
  29. Prouty A. M. , Van Velkinburgh J. C. , Gunn J. S. . ( 2002; ). Salmonella enterica serovar Typhimurium resistance to bile: identification and characterization of the tolQRA cluster. . J Bacteriol 184:, 1270–1276. [CrossRef] [PubMed]
    [Google Scholar]
  30. Suzuki H. , Nishimura Y. , Yasuda S. , Nishimura A. , Yamada M. , Hirota Y. . ( 1978; ). Murein-lipoprotein of Escherichia coli: a protein involved in the stabilization of bacterial cell envelope. . Mol Gen Genet 167:, 1–9.[PubMed]
    [Google Scholar]
  31. Walburger A. , Lazdunski C. , Corda Y. . ( 2002; ). The Tol/Pal system function requires an interaction between the C-terminal domain of TolA and the N-terminal domain of TolB. . Mol Microbiol 44:, 695–708. [CrossRef] [PubMed]
    [Google Scholar]
  32. Webster R. E. . ( 1991; ). The tol gene products and the import of macromolecules into Escherichia coli . . Mol Microbiol 5:, 1005–1011. [CrossRef] [PubMed]
    [Google Scholar]
  33. Yem D. W. , Wu H. C. . ( 1978; ). Physiological characterization of an Escherichia coli mutant altered in the structure of murein lipoprotein. . J Bacteriol 133:, 1419–1426.[PubMed]
    [Google Scholar]
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