1887

Abstract

, a Gram-negative bacterium belonging to the clade of the family , forms a mutualistic association with the soil nematode . The nematode invades insects and releases into the haemolymph, where it participates in insect killing. To begin to understand the role of fimbriae in the unique life cycle of , the organization and expression of the fimbrial operon was analysed. The operon contained only five structural genes (), making it one of the smallest chaperone-usher fimbrial operons studied to date. Unlike the operon of , a site-specific recombinase was not linked to the operon. The intergenic region between the major fimbrial gene () and the usher gene () lacked a -like gene, but contained three tandem inverted repeat sequences located downstream of . A 940 nt -containing mRNA was the major transcript produced in cells growing on agar, while an polycistronic mRNA was produced at low levels. A canonical promoter, identified upstream of , was not subject to promoter inversion. Fimbriae were not produced in an -mutant strain, suggesting that the leucine-responsive regulatory protein, Lrp, plays a role in the regulation of the operon. These findings show that the genetic organization and regulation of the operon is in several respects distinct from other chaperone-usher fimbrial operons.

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2004-05-01
2019-10-14
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References

  1. Alexeyev, M. F. ( 1999; ). The pKNOCK series of broad-host-range mobilizable suicide vectors for gene knockout and targeted DNA insertion into the chromosome of gram-negative bacteria. Biotechniques 26, 824–828.
    [Google Scholar]
  2. Bäga, M., Norgren, M. & Normark, S. ( 1987; ). Biogenesis of E. coli Pap pili: PapH, a minor pilin subunit involved in cell anchoring and length modulation. Cell 49, 241–251.[CrossRef]
    [Google Scholar]
  3. Bäga, M., Göransson, M., Normark, S. & Uhlin, B. E. ( 1988; ). Processed mRNA with differential stability in the regulation of E. coli pilin gene expression. Cell 52, 197–206.[CrossRef]
    [Google Scholar]
  4. Bailey, T. & Elkan, C. ( 1994; ). Fitting a mixture model by expectation maximization to discover motifs in biopolymers. In Proceedings of the Second International Conference on Intelligent Systems for Molecular Biology, pp. 28–36. Menlo Park, California: AAAI Press.
  5. Binnington, K. C. & Brooks, L. ( 1993; ). Fimbrial attachment of Xenorhabdus nematophilus to the intestine of Steinernema carpocapsae. In Nematodes and the Biological Control of Insect Pests, pp. 147–155. Edited by R. Bedding, R. Akhurst & H. Kaya. Melbourne, Australia: CSIRO Publications.
  6. Blomfield, I. C. ( 2001; ). The regulation of Pap and type 1 fimbriation in Escherichia coli. Adv Microb Physiol 45, 1–49.
    [Google Scholar]
  7. Connell, H., Agace, W., Klemm, P., Schembri, M., Mårild, S. & Svanborg, C. ( 1996; ). Type 1 fimbrial expression enhances Escherichia coli virulence for the urinary tract. Proc Natl Acad Sci U S A 93, 9827–9832.[CrossRef]
    [Google Scholar]
  8. Forst, S. & Nealson, K. ( 1996; ). Molecular biology of the symbiotic-pathogenic bacteria Xenorhabdus spp. and Photorhabdus spp. Microbiol Rev 60, 21–43.
    [Google Scholar]
  9. Forst, S. & Boylan, B. ( 2002; ). Characterization of the pleiotropic phenotype of an ompR strain of Xenorhabdus nematophila. Antonie van Leeuwenhoek 81, 43–49.[CrossRef]
    [Google Scholar]
  10. Forst, S. & Clarke, D. ( 2002; ). Bacteria-nematodes symbiosis. In Entomopathogenic Nematology, pp. 57–77. Edited by R. Gaugler. London: CABI Publishing.
  11. Forst, S., Dowds, B., Boemare, N. & Stackebrandt, E. ( 1997; ). Xenorhabdus and Photorhabdus spp.: bugs that kill bugs. Annu Rev Microbiol 51, 47–72.[CrossRef]
    [Google Scholar]
  12. Gally, D. L., Bogan, J. A., Eisenstein, B. I. & Blomfield, I. C. ( 1993; ). Environmental regulation of the fim switch controlling type 1 fimbrial phase variation in Escherichia coli K-12: effects of temperature and media. J Bacteriol 175, 6186–6193.
    [Google Scholar]
  13. Girardeau, J. P., Bertin, Y. & Callebaut, I. ( 2000; ). Conserved structural features in Class I major fimbrial subunits (pilin) in gram-negative bacteria. Molecular basis of classification in seven subfamilies and identification of intrasubfamily sequence signature motifs which might be implicated in quaternary structure. J Mol Evol 50, 424–442.
    [Google Scholar]
  14. Hacker, J. & Morschhäuser, J. ( 1994; ). S and F1C fimbriae. In Fimbriae: Adhesion, Genetics, Biogenesis and Vaccines, pp. 27–36. Edited by P. Klemm. Boca Raton, FL: CRC Press.
  15. He, H. ( 2002; ). Functional analysis of the mannose resistant fimbrial operon, mrx, in Xenorhabdus nematophila. PhD thesis, University of Wisconsin-Milwaukee.
  16. Hernday, A., Krabbe, M., Braaten, B. & Low, D. ( 2002; ). Self-perpetuating epigenic pili switches in bacteria. Proc Natl Acad Sci U S A 99, 16470–16476.[CrossRef]
    [Google Scholar]
  17. Heungens, K., Cowles, C. E. & Goodrich-Blair, H. ( 2002; ). Identification of Xenorhabdus nematophila genes required for mutualistic colonization of Steinernema carpocapsae nematodes. Mol Microbiol 45, 1337–1353.[CrossRef]
    [Google Scholar]
  18. Kim, D., Boylan, B., George, N. & Forst, S. ( 2003; ). Inactivation of ompR promotes precocious swarming and flhDC expression in Xenorhabdus nematophila. J Bacteriol 185, 5290–5294.[CrossRef]
    [Google Scholar]
  19. Li, X. & Mobley, H. L. T. ( 1998; ). MrpB functions as the terminator for the assembly of Proteus mirabilis mannose-resistant Proteus-like fimbriae. Infect Immun 66, 1759–1763.
    [Google Scholar]
  20. Li, X., Rasko, D. A., Lockatell, C. V., Johnson, D. E. & Mobley, H. L. T. ( 2001; ). Repression of bacterial motility by a novel fimbrial gene product. EMBO J 20, 4854–4862.[CrossRef]
    [Google Scholar]
  21. Low, D., Braaten, B. & Woude, M. V. D. ( 1996; ). Fimbriae. In Escherichia coli and Salmonella: Cellular and Molecular Biology, pp. 146–157. Edited by C. N. Frederick. Washington, DC: American Society for Microbiology.
  22. Meslet-Cladiere, L. M., Pimenta, A., Duchaud, E., Holland, I. B. & Blight, M. A. ( 2004; ). In vivo expression of mannose-resistant fimbriae of Photorhabdus temperata K122 during insect infection. J Bacteriol 186, 611–622.[CrossRef]
    [Google Scholar]
  23. Mol, O. & Oudega, B. ( 1996; ). Molecular and structural aspects of fimbriae biosynthesis and assembly in Escherichia coli. FEMS Microbiol Rev 19, 25–52.[CrossRef]
    [Google Scholar]
  24. Moureaux, N., Karjalainen, T., Givaudan, A., Bourlioux, P. & Boemare, N. ( 1995; ). Biochemical characterization and agglutinating properties of Xenorhabdus nematophilus F1 fimbriae. Appl Environ Microbiol 61, 2707–2712.
    [Google Scholar]
  25. Old, D. C. & Duguid, J. P. ( 1970; ). Selective outgrowth of fimbriate bacteria in static liquid medium. J Bacteriol 103, 447–456.
    [Google Scholar]
  26. Otto, K. & Silhavy, T. ( 2002; ). Surface sensing and adhesion of Escherichia coli controlled by the Cpx-signaling pathway. Proc Natl Acad Sci U S A 99, 2287–2292.[CrossRef]
    [Google Scholar]
  27. Prigent-Combaret, C., Brombacher, E., Vidal, O., Ambert, A., Lejeune, P., Landini, P. & Dorel, C. ( 2001; ). Complex regulatory network controls initial adhesion and biofilm formation in Escherichia coli via regulation of the csgD gene. J Bacteriol 183, 7213–7223.[CrossRef]
    [Google Scholar]
  28. Römling, U., Bian, Z., Hammer, M., Sierralta, W. D. & Normark, S. ( 1998; ). Curli fibers are highly conserved between Salmonella typhimurium and Escherichia coli with respect to operon structure and regulation. J Bacteriol 180, 722–731.
    [Google Scholar]
  29. Soto, G. E. & Hultgren, S. J. ( 1999; ). Bacterial adhesins: common themes and variations in architecture and assembly. J Bacteriol 181, 1059–1071.
    [Google Scholar]
  30. Stabb, E. V. & Ruby, E. G. ( 2003; ). Contribution of pilA to competitive colonization of the squid Euprymna scolopes by Vibrio fischeri. Appl Environ Microbiol 69, 820–826.[CrossRef]
    [Google Scholar]
  31. Stentebjerg-Olesen, B., Chakraborty, T. & Klemm, P. ( 1999; ). Type 1 fimbriation and phase switching in a natural Escherichia coli fimB null strain, Nissle 1917. J Bacteriol 181, 7470–7478.
    [Google Scholar]
  32. Tinker, J. K., Hancox, L. S. & Clegg, S. ( 2001; ). FimW is a negative regulator affecting type 1 fimbrial expression in Salmonella enterica serovar typhimurium. J Bacteriol 183, 435–442.[CrossRef]
    [Google Scholar]
  33. Tullus, K., Kuhn, I., Orskov, I., Orskov, F. & Mollby, R. ( 1992; ). The importance of P and type 1 fimbriae for the persistence of Escherichia coli in the human gut. Epidemiol Infect 108, 415–421.[CrossRef]
    [Google Scholar]
  34. Vivas, E. I. & Goodrich-Blair, H. ( 2001; ). Xenorhabdus nematophilus as a model for host-bacterium interactions: rpoS is necessary for mutualism with nematodes. J Bacteriol 183, 4687–4693.[CrossRef]
    [Google Scholar]
  35. Webster, J. M., Chen, G., Hu, K. & Li, J. ( 2002; ). Bacterial metabolites. In Entomopathogenic Nematology, pp. 99–114. Edited by R. Gaugler. London: CABI Publishing.
  36. Zhao, H., Li, X., Johnson, D. E., Blomfield, I. & Mobley, H. L. T. ( 1997; ). In vivo phase variation of MR/P fimbrial gene expression in Proteus mirabilis infecting the urinary tract. Mol Microbiol 23, 1009–1019.[CrossRef]
    [Google Scholar]
  37. Zhou, X., Kaya, H., Heungens, K. & Goodrich-Blair, H. ( 2002; ). Response of ants to a deterrent factor(s) produced by the symbiotic bacteria of entomopathogenic nematodes. Appl Environ Microbiol 68, 6202–6209.[CrossRef]
    [Google Scholar]
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