1887

Abstract

The twin-arginine translocase (Tat) complex is a unique system that translocates folded proteins across the cytoplasmic membrane. In this study, the Tat transporter system in was characterized to determine the role of Tat in the iron uptake pathway. A putative operon, containing conserved Fur-binding sequences in the promoter region, has been predicted to encode Tat-translocase components. Another operon, , with a putative Fur-binding sequence in the promoter, close to TatAC, was identified in the complementary strands of . Electrophoretic mobility shift assay showed that the listerial Fur-repressor binds to the promoter of the operon, suggesting that is under Fur regulation. Using a heterologous system in a reporter assay, FepB was translocated across the membrane. Mutations in and were constructed to determine the roles of Tat and FepB, respectively. In a whole-cell ferric reductase assay, the and mutants were found to have reduced levels of ferric reductase activities compared with those of the isogenic parent strain. Although ferric reductase activity has been demonstrated in , a conventional ferric reductase encoding sequence does not appear to be present in its genome. Hence, we propose that encodes a ferric reductase enzyme, which is translocated by the Tat-translocase system onto the bacterial cell surface, and plays an important role in the reductive iron uptake process in .

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.083642-0
2015-02-01
2024-11-11
Loading full text...

Full text loading...

/deliver/fulltext/micro/161/2/264.html?itemId=/content/journal/micro/10.1099/mic.0.083642-0&mimeType=html&fmt=ahah

References

  1. Adams T. J., Vartivarian S., Cowart R. E. 1990; Iron acquisition systems of Listeria monocytogenes. Infect Immun 58:2715–2718[PubMed]
    [Google Scholar]
  2. Alami M., Lüke I., Deitermann S., Eisner G., Koch H. G., Brunner J., Müller M. 2003; Differential interactions between a twin-arginine signal peptide and its translocase in Escherichia coli. Mol Cell 12:937–946 [View Article][PubMed]
    [Google Scholar]
  3. Andrews S. C., Robinson A. K., Rodríguez-Quiñones F. 2003; Bacterial iron homeostasis. FEMS Microbiol Rev 27:215–237 [View Article][PubMed]
    [Google Scholar]
  4. Bagg A., Neilands J. B. 1987; Ferric uptake regulation protein acts as a repressor, employing iron (II) as a cofactor to bind the operator of an iron transport operon in Escherichia coli. Biochemistry 26:5471–5477 [View Article][PubMed]
    [Google Scholar]
  5. Baichoo N., Helmann J. D. 2002; Recognition of DNA by Fur: a reinterpretation of the Fur box consensus sequence. J Bacteriol 184:5826–5832 [View Article][PubMed]
    [Google Scholar]
  6. Barker A. P., Vasil A. I., Filloux A., Ball G., Wilderman P. J., Vasil M. L. 2004; A novel extracellular phospholipase C of Pseudomonas aeruginosa is required for phospholipid chemotaxis. Mol Microbiol 53:1089–1098 [View Article][PubMed]
    [Google Scholar]
  7. Berks B. C., Palmer T., Sargent F. 2003; The Tat protein translocation pathway and its role in microbial physiology. Adv Microb Physiol 47:187–254 [View Article][PubMed]
    [Google Scholar]
  8. Biswas L., Biswas R., Nerz C., Ohlsen K., Schlag M., Schäfer T., Lamkemeyer T., Ziebandt A. K., Hantke K.& other authors ( 2009; Role of the twin-arginine translocation pathway in Staphylococcus. J Bacteriol 191:5921–5929 [View Article][PubMed]
    [Google Scholar]
  9. Brown J. S., Holden D. W. 2002; Iron acquisition by Gram-positive bacterial pathogens. Microbes Infect 4:1149–1156 [View Article][PubMed]
    [Google Scholar]
  10. Camejo A., Buchrieser C., Couvé E., Carvalho F., Reis O., Ferreira P., Sousa S., Cossart P., Cabanes D. 2009; In vivo transcriptional profiling of Listeria monocytogenes and mutagenesis identify new virulence factors involved in infection. PLoS Pathog 5:e1000449 [View Article][PubMed]
    [Google Scholar]
  11. Cao J., Woodhall M. R., Alvarez J., Cartron M. L., Andrews S. C. 2007; EfeUOB (YcdNOB) is a tripartite, acid-induced and CpxAR-regulated, low-pH Fe2+ transporter that is cryptic in Escherichia coli K-12 but functional in E. coli O157:H7. Mol Microbiol 65:857–875 [View Article][PubMed]
    [Google Scholar]
  12. Chakraborty T., Leimeister-Wächter M., Domann E., Hartl M., Goebel W., Nichterlein T., Notermans S. 1992; Coordinate regulation of virulence genes in Listeria monocytogenes requires the product of the prfA gene. J Bacteriol 174:568–574[PubMed]
    [Google Scholar]
  13. Charpentier E., Courvalin P. 1999; Antibiotic resistance in Listeria spp.. Antimicrob Agents Chemother 43:2103–2108[PubMed]
    [Google Scholar]
  14. Conte M. P., Longhi C., Polidoro M., Petrone G., Buonfiglio V., Di Santo S., Papi E., Seganti L., Visca P., Valenti P. 1996; Iron availability affects entry of Listeria monocytogenes into the enterocytelike cell line Caco-2. Infect Immun 64:3925–3929[PubMed]
    [Google Scholar]
  15. Cowart R. E. 2002; Reduction of iron by extracellular iron reductases: implications for microbial iron acquisition. Arch Biochem Biophys 400:273–281 [View Article][PubMed]
    [Google Scholar]
  16. Deneer H. G., Healey V., Boychuk I. 1995; Reduction of exogenous ferric iron by a surface-associated ferric reductase of Listeria spp.. Microbiology 141:1985–1992 [View Article][PubMed]
    [Google Scholar]
  17. Desvaux M., Hébraud M. 2006; The protein secretion systems in Listeria: inside out bacterial virulence. FEMS Microbiol Rev 30:774–805 [View Article][PubMed]
    [Google Scholar]
  18. Dilks K., Giménez M. I., Pohlschröder M. 2005; Genetic and biochemical analysis of the twin-arginine translocation pathway in halophilic archaea. J Bacteriol 187:8104–8113 [View Article][PubMed]
    [Google Scholar]
  19. Fallah A. A., Saei-Dehkordi S. S., Rahnama M., Tahmasby H., Mahzounieh M. 2012; Prevalence and antimicrobial resistance patterns of Listeria species isolated from poultry products marketed in Iran. Food Control 28:327–332 [View Article]
    [Google Scholar]
  20. Faraldo-Gómez J. D., Smith G. R., Sansom M. S. 2003; Molecular dynamics simulations of the bacterial outer membrane protein FhuA: a comparative study of the ferrichrome-free and bound states. Biophys J 85:1406–1420 [View Article][PubMed]
    [Google Scholar]
  21. Freitag N. E., Port G. C., Miner M. D. 2009; Listeria monocytogenes - from saprophyte to intracellular pathogen. Nat Rev Microbiol 7:623–628 [View Article][PubMed]
    [Google Scholar]
  22. Hantke K. 2001; Iron and metal regulation in bacteria. Curr Opin Microbiol 4:172–177 [View Article][PubMed]
    [Google Scholar]
  23. Hartford T., O’Brien S., Andrew P. W., Jones D., Roberts I. S. 1993; Utilization of transferrin-bound iron by Listeria monocytogenes. FEMS Microbiol Lett 108:311–318 [View Article][PubMed]
    [Google Scholar]
  24. Jin B., Newton S. M., Shao Y., Jiang X., Charbit A., Klebba P. E. 2006; Iron acquisition systems for ferric hydroxamates, haemin and haemoglobin in Listeria monocytogenes. Mol Microbiol 59:1185–1198 [View Article][PubMed]
    [Google Scholar]
  25. Jongbloed J. D., Antelmann H., Hecker M., Nijland R., Bron S., Airaksinen U., Pries F., Quax W. J., van Dijl J. M., Braun P. G. 2002; Selective contribution of the twin-arginine translocation pathway to protein secretion in Bacillus subtilis. J Biol Chem 277:44068–44078 [View Article][PubMed]
    [Google Scholar]
  26. Jongbloed J. D., Grieger U., Antelmann H., Hecker M., Nijland R., Bron S., van Dijl J. M. 2004; Two minimal Tat translocases in Bacillus. Mol Microbiol 54:1319–1325 [View Article][PubMed]
    [Google Scholar]
  27. Kuhn M., Goebel W. 1999; Pathogenesis of Listeria monocytogenes. In Listeria, Listeriosis, and Food Safety pp. 97–130 Edited by Ryser E. T., Marth E. H. New York: Marcel Dekker;
    [Google Scholar]
  28. Ledala N., Pearson S. L., Wilkinson B. J., Jayaswal R. K. 2007; Molecular characterization of the Fur protein of Listeria monocytogenes. Microbiology 153:1103–1111 [View Article][PubMed]
    [Google Scholar]
  29. Ledala N., Sengupta M., Muthaiyan A., Wilkinson B. J., Jayaswal R. K. 2010; Transcriptomic response of Listeria monocytogenes to iron limitation and Fur mutation. Appl Environ Microbiol 76:406–416 [View Article][PubMed]
    [Google Scholar]
  30. Lee J. W., Helmann J. D. 2006; The PerR transcription factor senses H2O2 by metal-catalysed histidine oxidation. Nature 440:363–367 [View Article][PubMed]
    [Google Scholar]
  31. Lee P. A., Tullman-Ercek D., Georgiou G. 2006; The bacterial twin-arginine translocation pathway. Annu Rev Microbiol 60:373–395 [View Article][PubMed]
    [Google Scholar]
  32. Lee V. T., Schneewind O. 2001; Protein secretion and the pathogenesis of bacterial infections. Genes Dev 15:1725–1752 [View Article][PubMed]
    [Google Scholar]
  33. Li H., Jacques P. E., Ghinet M. G., Brzezinski R., Morosoli R. 2005; Determining the functionality of putative Tat-dependent signal peptides in Streptomyces coelicolor A3(2) by using two different reporter proteins. Microbiology 151:2189–2198 [View Article][PubMed]
    [Google Scholar]
  34. Liu X., Du Q., Wang Z., Zhu D., Huang Y., Li N., Wei T., Xu S., Gu L. 2011; Crystal structure and biochemical features of EfeB/YcdB from Escherichia coli O157: ASP235 plays divergent roles in different enzyme-catalyzed processes. J Biol Chem 286:14922–14931 [View Article][PubMed]
    [Google Scholar]
  35. McDonough J. A., Hacker K. E., Flores A. R., Pavelka M. S. Jr, Braunstein M. 2005; The twin-arginine translocation pathway of Mycobacterium smegmatis is functional and required for the export of mycobacterial β-lactamases. J Bacteriol 187:7667–7679 [View Article][PubMed]
    [Google Scholar]
  36. McGann P., Ivanek R., Wiedmann M., Boor K. J. 2007; Temperature-dependent expression of Listeria monocytogenes internalin and internalin-like genes suggests functional diversity of these proteins among the listeriae. Appl Environ Microbiol 73:2806–2814 [View Article][PubMed]
    [Google Scholar]
  37. McLaughlin H. P., Hill C., Gahan C. G. 2011; The impact of iron on Listeria monocytogenes; inside and outside the host. Curr Opin Biotechnol 22:194–199 [View Article][PubMed]
    [Google Scholar]
  38. McLaughlin H. P., Xiao Q., Rea R. B., Pi H., Casey P. G., Darby T., Charbit A., Sleator R. D., Joyce S. A.& other authors ( 2012; A putative P-type ATPase required for virulence and resistance to haem toxicity in Listeria monocytogenes. PLoS ONE 7:e30928 [View Article][PubMed]
    [Google Scholar]
  39. Ochsner U. A., Snyder A., Vasil A. I., Vasil M. L. 2002; Effects of the twin-arginine translocase on secretion of virulence factors, stress response, and pathogenesis. Proc Natl Acad Sci U S A 99:8312–8317 [View Article][PubMed]
    [Google Scholar]
  40. Olsen K. N., Larsen M. H., Gahan C. G., Kallipolitis B., Wolf X. A., Rea R., Hill C., Ingmer H. 2005; The Dps-like protein Fri of Listeria monocytogenes promotes stress tolerance and intracellular multiplication in macrophage-like cells. Microbiology 151:925–933 [View Article][PubMed]
    [Google Scholar]
  41. Park S. F., Stewart G. S. 1990; High-efficiency transformation of Listeria monocytogenes by electroporation of penicillin-treated cells. Gene 94:129–132 [View Article][PubMed]
    [Google Scholar]
  42. Polidoro M., De Biase D., Montagnini B., Guarrera L., Cavallo S., Valenti P., Stefanini S., Chiancone E. 2002; The expression of the dodecameric ferritin in Listeria spp. is induced by iron limitation and stationary growth phase. Gene 296:121–128 [View Article][PubMed]
    [Google Scholar]
  43. Posey J. E., Shinnick T. M., Quinn F. D. 2006; Characterization of the twin-arginine translocase secretion system of Mycobacterium smegmatis. J Bacteriol 188:1332–1340 [View Article][PubMed]
    [Google Scholar]
  44. Rose R. W., Brüser T., Kissinger J. C., Pohlschröder M. 2002; Adaptation of protein secretion to extremely high-salt conditions by extensive use of the twin-arginine translocation pathway. Mol Microbiol 45:943–950 [View Article][PubMed]
    [Google Scholar]
  45. Sakaridis I., Soultos N., Iossifidou E., Papa A., Ambrosiadis I., Koidis P. 2011; Prevalence and antimicrobial resistance of Listeria monocytogenes isolated in chicken slaughterhouses in Northern Greece. J Food Prot 74:1017–1021 [View Article][PubMed]
    [Google Scholar]
  46. Schlech W. F. III 2000; Foodborne listeriosis. Clin Infect Dis 31:770–775 [View Article][PubMed]
    [Google Scholar]
  47. Shen A., Higgins D. E. 2006; The MogR transcriptional repressor regulates nonhierarchal expression of flagellar motility genes and virulence in Listeria monocytogenes. PLoS Pathog 2:e30 [View Article][PubMed]
    [Google Scholar]
  48. Singh V. K., Xiong A., Usgaard T. R., Chakrabarti S., Deora R., Misra T. K., Jayaswal R. K. 1999; ZntR is an autoregulatory protein and negatively regulates the chromosomal zinc resistance operon znt of Staphylococcus aureus. Mol Microbiol 33:200–207 [View Article][PubMed]
    [Google Scholar]
  49. van der Ploeg R., Barnett J. P., Vasisht N., Goosens V. J., Pöther D. C., Robinson C., van Dijl J. M. 2011; Salt sensitivity of minimal twin arginine translocases. J Biol Chem 286:43759–43770 [View Article][PubMed]
    [Google Scholar]
  50. Voulhoux R., Filloux A., Schalk I. J. 2006; Pyoverdine-mediated iron uptake in Pseudomonas aeruginosa: the Tat system is required for PvdN but not for FpvA transport. J Bacteriol 188:3317–3323 [View Article][PubMed]
    [Google Scholar]
  51. Walsh D., Duffy G., Sheridan J. J., Blair I. S., McDowell D. A. 2001; Antibiotic resistance among Listeria, including Listeria monocytogenes, in retail foods. J Appl Microbiol 90:517–522 [View Article][PubMed]
    [Google Scholar]
  52. Weinberg E. D. 2009; Iron availability and infection. Biochim Biophys Acta 1790:600–605 [View Article][PubMed]
    [Google Scholar]
  53. Widdick D. A., Dilks K., Chandra G., Bottrill A., Naldrett M., Pohlschröder M., Palmer T. 2006; The twin-arginine translocation pathway is a major route of protein export in Streptomyces coelicolor. Proc Natl Acad Sci U S A 103:17927–17932 [View Article][PubMed]
    [Google Scholar]
  54. Widdick D. A., Eijlander R. T., van Dijl J. M., Kuipers O. P., Palmer T. 2008; A facile reporter system for the experimental identification of twin-arginine translocation (Tat) signal peptides from all kingdoms of life. J Mol Biol 375:595–603 [View Article][PubMed]
    [Google Scholar]
  55. Xiao Q., Jiang X., Moore K. J., Shao Y., Pi H., Dubail I., Charbit A., Newton S. M., Klebba P. E. 2011; Sortase independent and dependent systems for acquisition of haem and haemoglobin in Listeria monocytogenes. Mol Microbiol 80:1581–1597 [View Article][PubMed]
    [Google Scholar]
  56. Xiong A., Singh V. K., Cabrera G., Jayaswal R. K. 2000; Molecular characterization of the ferric-uptake regulator, fur, from Staphylococcus aureus. Microbiology 146:659–668[PubMed]
    [Google Scholar]
  57. Yahr T. L., Wickner W. T. 2001; Functional reconstitution of bacterial Tat translocation in vitro. EMBO J 20:2472–2479 [View Article][PubMed]
    [Google Scholar]
/content/journal/micro/10.1099/mic.0.083642-0
Loading
/content/journal/micro/10.1099/mic.0.083642-0
Loading

Data & Media loading...

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