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. 1997 Mar;63(3):962–968. doi: 10.1128/aem.63.3.962-968.1997

Role of the histidine kinase, EnvZ, in the production of outer membrane proteins in the symbiotic-pathogenic bacterium Xenorhabdus nematophilus.

S A Forst 1, N Tabatabai 1
PMCID: PMC168388  PMID: 9055414

Abstract

We show that inactivation of envZ, the gene encoding the histidine kinase sensor protein, EnvZ, of Xenorhabdus nematophilus, affected the production of several outer membrane proteins (Opns). X. nematophilus produced five major Opns during exponential growth. Insertional inactivation of envZ led to a decrease in the production of OpnP, the OmpF-like pore-forming protein which constitutes approximately 50% of the total outer membrane protein in X. nematophilus. OpnA production was also reduced, while the remaining Opns were produced normally. During the transition to stationary phase, three new outer membrane proteins, OpnB, OpnS, and OpnX, were induced in the wild-type strain. The envZ-minus strain, ANT1, did not produce OpnB and OpnX, while OpnS was induced at markedly reduced levels. These results suggest that EnvZ was required for the high-level production of OpnP during exponential growth and may be involved in the production of OpnB, OpnS, and OpnX during stationary-phase growth. We also show that ANT1 was more pathogenic than the wild-type strain when as few as five cells were injected into the hemolymph of the larval stage of the tobacco hornworm (Manduca sexta). The larvae died before significant numbers of bacteria were detectable in the hemolymph. These results are discussed in relation to the role of EnvZ in the life cycle of X. nematophilus.

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Selected References

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  1. Akhurst R. J. Antibiotic activity of Xenorhabdus spp., bacteria symbiotically associated with insect pathogenic nematodes of the families Heterorhabditidae and Steinernematidae. J Gen Microbiol. 1982 Dec;128(12):3061–3065. doi: 10.1099/00221287-128-12-3061. [DOI] [PubMed] [Google Scholar]
  2. Akhurst R. J., Boemare N. E. A numerical taxonomic study of the genus Xenorhabdus (Enterobacteriaceae) and proposed elevation of the subspecies of X. nematophilus to species. J Gen Microbiol. 1988 Jul;134(7):1835–1845. doi: 10.1099/00221287-134-7-1835. [DOI] [PubMed] [Google Scholar]
  3. Forst S., Delgado J., Ramakrishnan G., Inouye M. Regulation of ompC and ompF expression in Escherichia coli in the absence of envZ. J Bacteriol. 1988 Nov;170(11):5080–5085. doi: 10.1128/jb.170.11.5080-5085.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Forst S., Nealson K. Molecular biology of the symbiotic-pathogenic bacteria Xenorhabdus spp. and Photorhabdus spp. Microbiol Rev. 1996 Mar;60(1):21–43. doi: 10.1128/mr.60.1.21-43.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Forst S., Waukau J., Leisman G., Exner M., Hancock R. Functional and regulatory analysis of the OmpF-like porin, OpnP, of the symbiotic bacterium Xenorhabdus nematophilus. Mol Microbiol. 1995 Nov;18(4):779–789. doi: 10.1111/j.1365-2958.1995.mmi_18040779.x. [DOI] [PubMed] [Google Scholar]
  6. Huang K. J., Schieberl J. L., Igo M. M. A distant upstream site involved in the negative regulation of the Escherichia coli ompF gene. J Bacteriol. 1994 Mar;176(5):1309–1315. doi: 10.1128/jb.176.5.1309-1315.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Leisman G. B., Waukau J., Forst S. A. Characterization and environmental regulation of outer membrane proteins in Xenorhabdus nematophilus. Appl Environ Microbiol. 1995 Jan;61(1):200–204. doi: 10.1128/aem.61.1.200-204.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Maxwell P. W., Chen G., Webster J. M., Dunphy G. B. Stability and Activities of Antibiotics Produced during Infection of the Insect Galleria mellonella by Two Isolates of Xenorhabdus nematophilus. Appl Environ Microbiol. 1994 Feb;60(2):715–721. doi: 10.1128/aem.60.2.715-721.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. McCleary W. R., Stock J. B., Ninfa A. J. Is acetyl phosphate a global signal in Escherichia coli? J Bacteriol. 1993 May;175(10):2793–2798. doi: 10.1128/jb.175.10.2793-2798.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Nikaido H. Porins and specific diffusion channels in bacterial outer membranes. J Biol Chem. 1994 Feb 11;269(6):3905–3908. [PubMed] [Google Scholar]
  11. Poinar G. O., Jr, Thomas G. M. Significance of Achromobacter nematophilus Poinar and Thomas (Achromobacteraceae: Eubacteriales) in the development of the nematode, DD-136 (Neoaplectana sp. Steinernematidae). Parasitology. 1966 May;56(2):385–390. doi: 10.1017/s0031182000070980. [DOI] [PubMed] [Google Scholar]
  12. Priefer U. B., Simon R., Pühler A. Extension of the host range of Escherichia coli vectors by incorporation of RSF1010 replication and mobilization functions. J Bacteriol. 1985 Jul;163(1):324–330. doi: 10.1128/jb.163.1.324-330.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Quandt J., Hynes M. F. Versatile suicide vectors which allow direct selection for gene replacement in gram-negative bacteria. Gene. 1993 May 15;127(1):15–21. doi: 10.1016/0378-1119(93)90611-6. [DOI] [PubMed] [Google Scholar]
  14. Rampersaud A., Harlocker S. L., Inouye M. The OmpR protein of Escherichia coli binds to sites in the ompF promoter region in a hierarchical manner determined by its degree of phosphorylation. J Biol Chem. 1994 Apr 29;269(17):12559–12566. [PubMed] [Google Scholar]
  15. Schmidt T. M., Bleakley B., Nealson K. H. Characterization of an Extracellular Protease from the Insect Pathogen Xenorhabdus luminescens. Appl Environ Microbiol. 1988 Nov;54(11):2793–2797. doi: 10.1128/aem.54.11.2793-2797.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Shi W., Li C., Louise C. J., Adler J. Mechanism of adverse conditions causing lack of flagella in Escherichia coli. J Bacteriol. 1993 Apr;175(8):2236–2240. doi: 10.1128/jb.175.8.2236-2240.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Shin S., Park C. Modulation of flagellar expression in Escherichia coli by acetyl phosphate and the osmoregulator OmpR. J Bacteriol. 1995 Aug;177(16):4696–4702. doi: 10.1128/jb.177.16.4696-4702.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Sundar L., Chang F. N. Antimicrobial activity and biosynthesis of indole antibiotics produced by Xenorhabdus nematophilus. J Gen Microbiol. 1993 Dec;139(12):3139–3148. doi: 10.1099/00221287-139-12-3139. [DOI] [PubMed] [Google Scholar]
  19. Tabatabai N., Forst S. Molecular analysis of the two-component genes, ompR and envZ, in the symbiotic bacterium Xenorhabdus nematophilus. Mol Microbiol. 1995 Aug;17(4):643–652. doi: 10.1111/j.1365-2958.1995.mmi_17040643.x. [DOI] [PubMed] [Google Scholar]
  20. Xu J., Olson M. E., Kahn M. L., Hurlbert R. E. Characterization of Tn5-Induced Mutants of Xenorhabdus nematophilus ATCC 19061. Appl Environ Microbiol. 1991 Apr;57(4):1173–1180. doi: 10.1128/aem.57.4.1173-1180.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]

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