Advertisement

Antonie van Leeuwenhoek

, 81:43 | Cite as

Characterization of the pleiotropic phenotype of an ompR strain of Xenorhabdus nematophila

  • Steven ForstEmail author
  • Brian Boylan
Article

Abstract

Xenorhabdus nematophila is an insect pathogen that forms a symbiotic association with the nematode, Steinernema carpocapsae. Xenorhabdus is carried into the insect host by the nematode, is released into the hemolymph and participates in killing the insect. The bacteria grow to high concentrations supporting the development of the nematode in the hemolymph. OmpR is a global regulatory protein involved in the regulation of porin genes, motility, acid tolerance and virulence in several enteric bacteria. To study the role of ompR in the lifecyle of Xenorhabdus, an ompR -minus strain was constructed. The ompR strain produced markedly reduced levels of the porin protein, OpnP and was both hypermotile and exhibited a hyperhemolysis phenotype. Inactivation of flhDC, the master regulator for flagella synthesis, eliminated hemolysin production in the ompR strain, suggesting that ompR regulates hemolysin production via flhDC. The ompR mutant strain was virulent towards insect hosts. However, when nematodes were grown on a mixture of the wild-type and the ompR strain, only the wild-type strain was recovered indicating that ompR is required for competitive symbiotic interaction with the nematode. The role of ompR in the symbiosis between the bacterium and the nematode is under investigation.

global regulation flhDC ompR opnP symbiosis Xenorhabdus nematophila 

References

  1. Bang IS, Kim BH, Foster JW & Park YK (2000) OmpR regulates the stationary-phase acid tolerance response of Salmonella enterica serovar Typhimurium. J. Bacteriol. 182: 2245–2252.PubMedCrossRefGoogle Scholar
  2. Dorrell N, Li S-R, Everest PH, Dougan G & Wren BW (1998) Construction and characteization of a Yersinia entercolitica 0:8 ompR mutant. FEMS Micro. Lett. 164: 145–151.CrossRefGoogle Scholar
  3. Forst S, Waukau J, Leisman G, Exner M & Hancock J (1995) Functional and regulatory analysis of the OmpF-Iike porin, OpnP, of the symbiotic bacterium Xenorhabdus nematophila. Mol. Microbiol. 18: 779–789.PubMedCrossRefGoogle Scholar
  4. Forst S, Dowds B, Boemare N & Stackebrandt F (1997a) Xenorhabdus spp. and Photorhabdus spp.: bugs that kill bugs Anm. Rev. Microbiol. 51: 47–72.CrossRefGoogle Scholar
  5. Forst S, Tabatabai N (1997b) Role of the histidine kinase, EnvZ, in the production of outer membrane proteins in the symbioticpathogenic bacterium, Xenorhabdus nematophila. Appl. Environ. Microbiol. 63: 962–968.PubMedGoogle Scholar
  6. Givaudan A & Lanois A (2000) flhDC, the flagellar master operon of Xenorhabdus nematophila: requirement for motility, lipolysis, extracellular hemolysis and full virulence in insects, J. Bacteriol. 182: 107–115PubMedCrossRefGoogle Scholar
  7. Kalogeralci VS & Winans SC (1997) Suicide plasmids containing promoterless reporter genes can simultaneously disrupt and create fusions to target genes of diverse bacteria. Gene 188: 69–75.CrossRefGoogle Scholar
  8. Lindgren, SW, Stojiljkovic L & Heifron F (1996) Macrophage killing is an essential virulence mechanism of Salmonella typhimurium. Proc. Natl. Acad. Sci. USA 93: 4197–4201.PubMedCrossRefGoogle Scholar
  9. Lee AK, Detweiler CS & Falkow S (2000) OmpR regulates the two-component system SsrA-SsrB in Salmonella pathogenicity island 2. J. Bacteriol. 182: 771–781.PubMedCrossRefGoogle Scholar
  10. Nikaido H (1994) Prevention of drug access to bacterial targets: permeability barrier and active efflux, Science 264: 382–388.PubMedGoogle Scholar
  11. Pratt LA & Silhavy TJ (1995) Porin Regulon of Escherichia coli In: Hoch JA & Silhavy TJ (Eds) Two-Component Signal Transduction (pp 105–127). ASM, Washington, D.C.Google Scholar
  12. Pruss BM (1998) Acetyl phosphate and the phosphorylation of OmpR are involved in the regulation of the cell division rate in Escherchia coli. Arch Microbiol. 170: 141–146PubMedCrossRefGoogle Scholar
  13. Pruss BM, Lui X, Hendrickson W & Matsumura P (2001) FlhD/FlhC-regulated promoters analyzed by gene array and lacZ gene fusions. ELMS Micro Lett. 197: 91–97.CrossRefGoogle Scholar
  14. Rampersaud A & Inouye M (1991) Procaine, a local anesthetic, signals through the EnvZ receptor to change the DNA binding affinity of the transcriptional activator protein OmpR. J. Bacteriol, 173: 6882–6888.PubMedGoogle Scholar
  15. Roberts DL, Bennett DW & Forst SA (1994) Identification of the site of phosphorylation on the osmosensor, EnvZ, of Escherichia coli. J. Biol. Chem. 269: 8728–8733.PubMedGoogle Scholar
  16. Russo ED & Silhavy TJ (1991) EnvZ controls the concentration of phosphorylated OmpR to mediate osmoregulation of the porin genes. J. Mol. Biol. 222: 567–580.Google Scholar
  17. Shin A & Park C (1995) Modulation of flagellar expression in Escherichia coli by acetyl phosphate and the osmoregulator OmpR. J. Bacteriol. 177: 4696–4702.PubMedGoogle Scholar
  18. Tabatabai N & Forst S (1995) Molecular analysis of the signal transduction genes, ompR and envZ, in the symbiotic bacteria, Xenorhabdus nematophila. Mol. Microbiol. 17: 643–652.PubMedCrossRefGoogle Scholar
  19. Vidal O, Longin R, Prigent-Combaret C, Dorel C, Hooreman M & Lejeune p (1998) Isolation of an Escherichia coli K-12 mutant strain able to form biofilms on inert surfaces: involvement of a new ompR allele that increases Curli expression. J. Bacteriol. 180: 2442–2449.PubMedGoogle Scholar
  20. Volgyi A, Fodor A, Szentirmai A & Forst S (1998) Phase variation in Xenorhabdus nematophila. Appl. Environ. Microbiol. 64: 1188–1193.PubMedGoogle Scholar
  21. Volgyi A, Fodor A & Forst S (2000) Inactivation of a novel gene produces a phenotypic variant cell and affects the symbiotic behavior of Xenorhabdus nematophila. Appl. Environ. Microbiol. 66: 1622–1628.PubMedCrossRefGoogle Scholar
  22. Young GM, Schmiel DH & Miller VL (1999) A new pathway for the secretion of virulence factors by bacteria: The flagellar export apparatus functions as a protein-secretion system. Proc. Nati. Acad. Sci. (USA) 96: 6456–6461.CrossRefGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2002

Authors and Affiliations

  1. 1.Department of Biological SciencesUniversity of WisconsinMilwaukeeUSA

Personalised recommendations