1887

Abstract

Enterohaemorrhagic (EHEC) is a gastrointestinal pathogen that causes diarrhoea and more severe diseases in humans. A key feature of EHEC is the type III secretion system (TTSS), which translocates virulence factors (effectors) directly into host cells. In this study, the expression and secretion of effectors in EHEC grown under anaerobic conditions were examined. The secretion of effectors was greatly enhanced, without an increase in their expression levels, when EHEC was grown in the presence of specific electron acceptors, such as trimethylamine -oxide (TMAO) and nitrate, for anaerobic respiration. The activation of the TTSS was dependent on the activity of respiratory systems, including electron-acceptor-specific signalling systems and reductases. Although protein synthesis was not required for TTSS activation, the inhibition of respiratory activity abolished secretion. EHEC grown with either TMAO or nitrate possessed a more intact type III secretion (TTS) apparatus, including the needle protein EscF and the translocator protein EspA, than EHEC grown without an electron acceptor. These observations suggest that activation of either the TMAO- or the nitrate-specific respiratory system accelerates the maturation of functional TTS apparatus under anaerobic growth conditions.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2006/000893-0
2007-02-01
2020-10-24
Loading full text...

Full text loading...

/deliver/fulltext/micro/153/2/464.html?itemId=/content/journal/micro/10.1099/mic.0.2006/000893-0&mimeType=html&fmt=ahah

References

  1. Ansaldi M., Bordi C., Lepelletier M., Mejean V.. 1999; TorC apocytochrome negatively autoregulates the trimethylamine N -oxide (TMAO) reductase operon in Escherichia coli . Mol Microbiol33:284–295[CrossRef]
    [Google Scholar]
  2. Beltrametti F., Kresse A. U., Guzman C. A.. 1999; Transcriptional regulation of the esp genes of enterohemorrhagic Escherichia coli . J Bacteriol181:3409–3418
    [Google Scholar]
  3. Blasco F., Iobbi C., Ratouchniak J., Bonnefoy V., Chippaux M.. 1990; Nitrate reductases of Escherichia coli : sequence of the second nitrate reductase and comparison with that encoded by the narGHJI operon. Mol Gen Genet222:104–111
    [Google Scholar]
  4. Darwin A. J., Stewart V.. 1995; Nitrate and nitrite regulation of the Fnr-dependent aeg-46.5 promoter of Escherichia coli K-12 is mediated by competition between homologous response regulators (NarL and NarP) for a common DNA-binding site. J Mol Biol251:15–29[CrossRef]
    [Google Scholar]
  5. Darwin A. J., Li J., Stewart V.. 1996; Analysis of nitrate regulatory protein NarL-binding sites in the fdnG and narG operon control regions of Escherichia coli K-12. Mol Microbiol20:621–632[CrossRef]
    [Google Scholar]
  6. Darwin A. J., Ziegelhoffer E. C., Kiley P. J., Stewart V.. 1998; Fnr, NarP, and NarL regulation of Escherichia coli K-12 napF (periplasmic nitrate reductase) operon transcription in vitro . J Bacteriol180:4192–4198
    [Google Scholar]
  7. 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 A97:6640–6645[CrossRef]
    [Google Scholar]
  8. Deng W., Puente J. L., Gruenheid S., Li Y., Vallance B. A., Vazquez A., Barba J., Ibarra J. A., O'Donnell P.. other authors 2004; Dissecting virulence: systematic and functional analyses of a pathogenicity island. Proc Natl Acad Sci U S A101:3597–3602[CrossRef]
    [Google Scholar]
  9. Eichelberg K., Ginocchio C. C., Galan J. E.. 1994; Molecular and functional characterization of the Salmonella typhimurium invasion genes invB and invC : homology of InvC to the F0F1 ATPase family of proteins. J Bacteriol176:4501–4510
    [Google Scholar]
  10. Frankel G., Phillips A. D., Rosenshine I., Dougan G., Kaper J. B., Knutton S.. 1998; Enteropathogenic and enterohaemorrhagic Escherichia coli : more subversive elements. Mol Microbiol30:911–921[CrossRef]
    [Google Scholar]
  11. Galan J. E., Collmer A.. 1999; Type III secretion machines: bacterial devices for protein delivery into host cells. Science284:1322–1328[CrossRef]
    [Google Scholar]
  12. Garmendia J., Frankel G., Crepin V. F.. 2005; Enteropathogenic and enterohemorrhagic Escherichia coli infections: translocation, translocation, translocation. Infect Immun73:2573–2585[CrossRef]
    [Google Scholar]
  13. Gauthier A., Puente J. L., Finlay B. B.. 2003; Secretin of the enteropathogenic Escherichia coli type III secretion system requires components of the type III apparatus for assembly and localization. Infect Immun71:3310–3319[CrossRef]
    [Google Scholar]
  14. Georgellis D., Kwon O., Lin E. C.. 2001; Quinones as the redox signal for the arc two-component system of bacteria. Science292:2314–2316[CrossRef]
    [Google Scholar]
  15. Hartland E. L., Daniell S. J., Delahay R. M., Neves B. C., Wallis T., Shaw R. K., Hale C., Knutton S., Frankel G.. 2000; The type III protein translocation system of enteropathogenic Escherichia coli involves EspA–EspB protein interactions. Mol Microbiol35:1483–1492
    [Google Scholar]
  16. Hayashi T., Makino K., Ohnishi M., Kurokawa K., Ishii K., Yokoyama K., Han C.-G., Ohtsubo E., Nakayama K., Murata T.. other authors 2001; Complete genome sequence of enterohemorrhagic Escherichia coli O157 : H7 and genomic comparison with laboratory strain K-12. DNA Res8:11–22[CrossRef]
    [Google Scholar]
  17. He S. Y., Nomura K., Whittam T. S.. 2004; Type III protein secretion mechanism in mammalian and plant pathogens. Biochim Biophys Acta 1694;181–206[CrossRef]
    [Google Scholar]
  18. Hueck C. J.. 1998; Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol Mol Biol Rev62:379–433
    [Google Scholar]
  19. Ide T., Laarmann S., Greune L., Schillers H., Oberleithner H., Schmidt M. A.. 2001; Characterization of translocation pores inserted into plasma membranes by type III-secreted Esp proteins of enteropathogenic Escherichia coli . Cell Microbiol3:669–679[CrossRef]
    [Google Scholar]
  20. Jackson M. W., Plano G. V.. 1999; DsbA is required for stable expression of outer membrane protein YscC and for efficient Yop secretion in Yersinia pestis . J Bacteriol181:5126–5130
    [Google Scholar]
  21. Kenny B., Abe A., Stein M., Finlay B. B.. 1997; Enteropathogenic Escherichia coli protein secretion is induced in response to conditions similar to those in the gastrointestinal tract. Infect Immun65:2606–2612
    [Google Scholar]
  22. Knutton S., Rosenshine I., Pallen M. J., Nisan I., Neves B. C., Bain C., Wolff C., Dougan G., Frankel G.. 1998; A novel EspA-associated surface organelle of enteropathogenic Escherichia coli involved in protein translocation into epithelial cells. Embo J17:2166–2176[CrossRef]
    [Google Scholar]
  23. Kubori T., Matsushima Y., Nakamura D., Uralil J., Lara-Tejero M., Sukhan A., Galan J. E., Aizawa S. I.. 1998; Supramolecular structure of the Salmonella typhimurium type III protein secretion system. Science280:602–605[CrossRef]
    [Google Scholar]
  24. Laemmli U. K.. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature227:680–685[CrossRef]
    [Google Scholar]
  25. Lee P. T., Hsu A. Y., Ha H. T., Clarke C. F.. 1997; A C -methyltransferase involved in both ubiquinone and menaquinone biosynthesis: isolation and identification of the Escherichia coli ubiE gene. J Bacteriol179:1748–1754
    [Google Scholar]
  26. Malpica R., Franco B., Rodriguez C., Kwon O., Georgellis D.. 2004; Identification of a quinone-sensitive redox switch in the ArcB sensor kinase. Proc Natl Acad Sci U S A101:13318–13323[CrossRef]
    [Google Scholar]
  27. Marlovits T. C., Kubori T., Sukhan A., Thomas D. R., Galan J. E., Unger V. M.. 2004; Structural insights into the assembly of the type III secretion needle complex. Science306:1040–1042[CrossRef]
    [Google Scholar]
  28. Mejean V., Iobbi-Nivol C., Lepelletier M., Giordano G., Chippaux M., Pascal M. C.. 1994; TMAO anaerobic respiration in Escherichia coli : involvement of the tor operon. Mol Microbiol11:1169–1179[CrossRef]
    [Google Scholar]
  29. Miki T., Okada N., Danbara H.. 2004; Two periplasmic disulfide oxidoreductases, DsbA and SrgA, target outer membrane protein SpiA, a component of the Salmonella pathogenicity island 2 type III secretion system. J Biol Chem279:34631–34642[CrossRef]
    [Google Scholar]
  30. Moon H. W., Whipp S. C., Argenzio R. A., Levine M. M., Giannella R. A.. 1983; Attaching and effacing activities of rabbit and human enteropathogenic Escherichia coli in pig and rabbit intestines. Infect Immun41:1340–1351
    [Google Scholar]
  31. Nataro J. P., Kaper J. B.. 1998; Diarrheagenic Escherichia coli . Clin Microbiol Rev11:142–201
    [Google Scholar]
  32. O'Connell C. B., Creasey E. A., Knutton S., Elliott S., Crowther L. J., Luo W., Albert M. J., Kaper J. B., Frankel G., Donnenberg M. S.. 2004; SepL, a protein required for enteropathogenic Escherichia coli type III translocation, interacts with secretion component SepD. Mol Microbiol52:1613–1625[CrossRef]
    [Google Scholar]
  33. Ogura Y., Kurokawa K., Ooka T., Tashiro K., Tobe T., Ohnishi M., Nakayama K., Morimoto T., Terajima J.. other authors 2006; Complexity of the genomic diversity in enterohemorrhagic Escherichia coli O157 revealed by the combinational use of the O157 Sakai oligoDNA microarray and the whole genome PCR scanning. DNA Res13:3–14[CrossRef]
    [Google Scholar]
  34. Ohnishi M., Terajima J., Kurokawa K., Nakayama K., Murata T., Tamura K., Ogura Y., Watanabe H., Hayashi T.. 2002; Genomic diversity of enterohemorrhagic Escherichia coli O157 revealed by whole genome PCR scanning. Proc Natl Acad Sci U S A99:17043–17048[CrossRef]
    [Google Scholar]
  35. Pommier J., Mejean V., Giordano G., Iobbi-Nivol C.. 1998; TorD, a cytoplasmic chaperone that interacts with the unfolded trimethylamine N -oxide reductase enzyme (TorA) in Escherichia coli . J Biol Chem273:16615–16620[CrossRef]
    [Google Scholar]
  36. Schagger H., von Jagow G.. 1987; Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem166:368–379[CrossRef]
    [Google Scholar]
  37. Schauer D. B., Falkow S.. 1993; Attaching and effacing locus of a Citrobacter freundii biotype that causes transmissible murine colonic hyperplasia. Infect Immun61:2486–2492
    [Google Scholar]
  38. Sekiya K., Ohishi M., Ogino T., Tamano K., Sasakawa C., Abe A.. 2001; Supermolecular structure of the enteropathogenic Escherichia coli type III secretion system and its direct interaction with the EspA-sheath-like structure. Proc Natl Acad Sci U S A98:11638–11643[CrossRef]
    [Google Scholar]
  39. Shalel-Levanon S., San K. Y., Bennett G. N.. 2005; Effect of ArcA and FNR on the expression of genes related to the oxygen regulation and the glycolysis pathway in Escherichia coli under microaerobic growth conditions. Biotechnol Bioeng92:147–159[CrossRef]
    [Google Scholar]
  40. Stevenson K. S. D., Meganathan R., Hudspeth M. E.. 1998; Menaquinone (vitamin K2) biosynthesis: localization and characterization of the menA gene from Escherichia coli . J Bacteriol180:2782–2787
    [Google Scholar]
  41. Stewart V.. 2003; Biochemical Society Special Lecture. Nitrate- and nitrite-responsive sensors NarX and NarQ of proteobacteria. Biochem Soc Trans31:1–10
    [Google Scholar]
  42. Tatsuno I., Kimura H., Okutani A., Kanamura K., Abe H., Nagai S., Makino K., Shinagawa H., Yoshida M.. other authors 2000; Isolation and characterization of mini-Tn 5 Km2 insertion mutants of enterohemorrhagic Escherichia coli O157 : H7 deficient in adherence to Caco-2 cells. Infect Immun68:5943–5952[CrossRef]
    [Google Scholar]
  43. Tzipori S., Gunzer F., Donnenberg M. S., Kaper J. B., Donohue-Rolfe A., de Montigny L.. 1995; The role of the eaeA gene in diarrhea and neurological complications in a gnotobiotic piglet model of enterohemorrhagic Escherichia coli infection. Infect Immun63:3621–3627
    [Google Scholar]
  44. Walker M. S., DeMoss J. A.. 1994; NarL-phosphate must bind to multiple upstream sites to activate transcription from the narG promoter of Escherichia coli . Mol Microbiol14:633–641[CrossRef]
    [Google Scholar]
  45. Watarai M., Tobe T., Yoshikawa M., Sasakawa C.. 1995; Disulfide oxidoreductase activity of Shigella flexneri is required for release of Ipa proteins and invasion of epithelial cells. Proc Natl Acad Sci U S A92:4927–4931[CrossRef]
    [Google Scholar]
  46. Wilson R. K., Shaw R. K., Daniell S., Knutton S., Frankel G.. 2001; Role of EscF, a putative needle complex protein, in the type III protein translocation system of enteropathogenic Escherichia coli . Cell Microbiol3:753–762[CrossRef]
    [Google Scholar]
  47. Wissenbach U., Ternes D., Unden G.. 1992; An Escherichia coli mutant containing only demethylmenaquinone, but no menaquinone: effects on fumarate, dimethylsulfoxide, trimethylamine N -oxide and nitrate respiration. Arch Microbiol158:68–73[CrossRef]
    [Google Scholar]
  48. Woestyn S., Allaoui A., Wattiau P., Cornelis G. R.. 1994; YscN, the putative energizer of the Yersinia Yop secretion machinery. J Bacteriol176:1561–1569
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2006/000893-0
Loading
/content/journal/micro/10.1099/mic.0.2006/000893-0
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

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