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Volume 166, Issue 4

The signaling peptide PapR is required for the activity of the quorum-sensor PlcRa in Free

Abstract

The transcriptional regulator PlcR, its cognate cell-cell signaling heptapeptide PapR, and the oligopeptide permease OppABCDF, required for PapR import, form a quorum-sensing system that controls the expression of virulence factors in and species. In strain ATCC 14579, the transcriptional regulator PlcRa activates the expression of gene, which encodes an AbrB-like transcriptional regulator involved in cysteine biosynthesis. PlcRa is a structural homolog of PlcR: in particular, its C-terminal TPR peptide-binding domain could be similarly arranged as in PlcR. The signaling peptide of PlcRa is not known. As PlcRa is a PlcR-like protein, the cognate PapR peptide (ADLPFEF) is a relevant candidate to act as a signaling peptide for PlcRa activation. Also, the putative PapRa peptide (CSIPYEY), encoded by the gene adjacent to the gene, is a relevant candidate as addition of synthetic PapRa induces a dose-dependent increase of expression. To address the issue of peptide selectivity of PlcRa, the role of PapR and PapRa peptides in PlcRa activity was investigated in 407 strain, by genetic and functional complementation analyses. A transcriptional fusion between the promoter of and was used to monitor the PlcRa activity in various genetic backgrounds. We demonstrated that PapR was necessary and sufficient for PlcRa activity. We showed that synthetic PapRs from pherogroups II, III and IV and synthetic PapRa were able to trigger expression, suggesting that PlcRa is less selective than PlcR. Lastly, the mode of binding of PlcRa was addressed using an approach. Overall, we report a new role for PapR as a signaling peptide for PlcRa activity and show a functional link between PlcR and PlcRa regulons in .

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  • Published Online:
Keyword(s): PapR peptide , peptide cross-talk , PlcRa regulator , quorum-sensing and RNPP regulators
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2020-01-28
2024-04-24
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References

  1. Waters CM, Bassler BL. Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 2005; 21:319–346 [View Article][PubMed]
     [Google Scholar]
  2. Neiditch MB, Capodagli GC, Prehna G, Federle MJ. Genetic and structural analyses of RRNPP intercellular peptide signaling of Gram-positive bacteria. Annu Rev Genet 2017; 51:311–333 [View Article][PubMed]
     [Google Scholar]
  3. Slamti L, Perchat S, Huillet E, Lereclus D. Quorum sensing in Bacillus thuringiensis is required for completion of a full infectious cycle in the insect. Toxins 2014; 6:2239–2255 [View Article][PubMed]
     [Google Scholar]
  4. Do H, Kumaraswami M. Structural mechanisms of peptide recognition and allosteric modulation of gene regulation by the RRNPP family of quorum-sensing regulators. J Mol Biol 2016; 428:2793–2804 [View Article][PubMed]
     [Google Scholar]
  5. Declerck N, Bouillaut L, Chaix D, Rugani N, Slamti L et al. Structure of plcR: insights into virulence regulation and evolution of quorum sensing in Gram-positive bacteria. Proc Natl Acad Sci U S A 2007; 104:18490–18495 [View Article][PubMed]
     [Google Scholar]
  6. Parashar V, Aggarwal C, Federle MJ, Neiditch MB. Rgg protein structure-function and inhibition by cyclic peptide compounds. Proc Natl Acad Sci U S A 2015; 112:5177–5182 [View Article][PubMed]
     [Google Scholar]
  7. Cardoso PdeF, Perchat S, Vilas-Boas LA, Lereclus D, Vilas-Bôas GT. Diversity of the Rap-Phr quorum-sensing systems in the Bacillus cereus group. Curr Genet 2019; 65:13671381 [View Article][PubMed]
     [Google Scholar]
  8. Ehling-Schulz M, Lereclus D, Koehler TM. The Bacillus cereus Group: Bacillus Species with Pathogenic Potential. Microbiol Spectr 2019; 7: [View Article][PubMed]
     [Google Scholar]
  9. Kolstø AB, Lereclus D, Mock M. Genome structure and evolution of the Bacillus cereus group. Curr Top Microbiol Immunol 2002; 264:95–108[PubMed]
     [Google Scholar]
  10. Agaisse H, Gominet M, Økstad OA, Kolstø AB, Lereclus D. PlcR is a pleiotropic regulator of extracellular virulence factor gene expression in Bacillus thuringiensis . Mol Microbiol 1999; 32:1043–1053 [View Article][PubMed]
     [Google Scholar]
  11. Salamitou S, Ramisse F, Brehélin M, Bourguet D, Gilois N et al. The plcR regulon is involved in the opportunistic properties of Bacillus thuringiensis and Bacillus cereus in mice and insects. Microbiology 2000; 146:2825–2832 [View Article][PubMed]
     [Google Scholar]
  12. Gohar M, Faegri K, Perchat S, Ravnum S, Økstad OA et al. The PlcR virulence regulon of Bacillus cereus . PLoS One 2008; 3:e2793 [View Article][PubMed]
     [Google Scholar]
  13. Buisson C, Gohar M, Huillet E, Nielsen-LeRoux C. Bacillus thuringiensis spores and vegetative bacteria: infection capacity and role of the virulence regulon PlcR following intrahaemocoel injection of Galleria mellonella . Insects 2019; 10:129 [View Article][PubMed]
     [Google Scholar]
  14. Slamti L, Lereclus D. A cell-cell signaling peptide activates the plcR virulence regulon in bacteria of the Bacillus cereus group. EMBO J 2002; 21:4550–4559 [View Article][PubMed]
     [Google Scholar]
  15. Grenha R, Slamti L, Nicaise M, Refes Y, Lereclus D et al. Structural basis for the activation mechanism of the plcR virulence regulator by the quorum-sensing signal peptide PapR. Proc Natl Acad Sci U S A 2013; 110:1047–1052 [View Article][PubMed]
     [Google Scholar]
  16. Bouillaut L, Perchat S, Arold S, Zorrilla S, Slamti L et al. Molecular basis for group-specific activation of the virulence regulator plcR by PapR heptapeptides. Nucleic Acids Res 2008; 36:3791–3801 [View Article][PubMed]
     [Google Scholar]
  17. Gominet M, Slamti L, Gilois N, Rose M, Lereclus D. Oligopeptide permease is required for expression of the Bacillus thuringiensis plcR regulon and for virulence. Mol Microbiol 2001; 40:963–975 [View Article][PubMed]
     [Google Scholar]
  18. Slamti L, Lemy C, Henry C, Guillot A, Huillet E et al. CodY regulates the activity of the virulence quorum sensor PlcR by controlling the import of the signaling peptide PapR in Bacillus thuringiensis . Front Microbiol 2015; 6:1501 [View Article][PubMed]
     [Google Scholar]
  19. Frenzel E, Doll V, Pauthner M, Lücking G, Scherer S et al. CodY orchestrates the expression of virulence determinants in emetic Bacillus cereus by impacting key regulatory circuits. Mol Microbiol 2012; 85:67–88 [View Article][PubMed]
     [Google Scholar]
  20. Lindbäck T, Mols M, Basset C, Granum PE, Kuipers OP et al. Cody, a pleiotropic regulator, influences multicellular behaviour and efficient production of virulence factors in Bacillus cereus . Environ Microbiol 2012; 14:2233–2246 [View Article][PubMed]
     [Google Scholar]
  21. Slamti L, Lereclus D. Specificity and polymorphism of the PlcR-PapR quorum-sensing system in the Bacillus cereus group. J Bacteriol 2005; 187:1182–1187 [View Article][PubMed]
     [Google Scholar]
  22. Huillet E, Tempelaars MH, André-Leroux G, Wanapaisan P, Bridoux L et al. PlcRa, a new quorum-sensing regulator from Bacillus cereus, plays a role in oxidative stress responses and cysteine metabolism in stationary phase. PLoS One 2012; 7:e51047 [View Article][PubMed]
     [Google Scholar]
  23. Huillet E, Gohar M. Quorum sensing in Bacillus cereus in relation with cysteine metabolism and oxidative stress response. In de Bruijn FJ. editor Stress and Environmental Regulation of Gene Expression and Adaptation in Bacteria, 2. Wiley; 2016 pp 1242–1251
     [Google Scholar]
  24. Dubois T, Faegri K, Perchat S, Lemy C, Buisson C et al. Necrotrophism is a quorum-sensing-regulated lifestyle in Bacillus thuringiensis . PLoS Pathog 2012; 8:e1002629 [View Article][PubMed]
     [Google Scholar]
  25. Ivanova N, Sorokin A, Anderson I, Galleron N, Candelon B et al. Genome sequence of Bacillus cereus and comparative analysis with Bacillus anthracis . Nature 2003; 423:87–91 [View Article][PubMed]
     [Google Scholar]
  26. Lereclus D, Arantes O, Chaufaux J, Lecadet M. Transformation and expression of a cloned delta-endotoxin gene in Bacillus thuringiensis . FEMS Microbiol Lett 1989; 51:211–217 [View Article][PubMed]
     [Google Scholar]
  27. Guinebretière M-H, Thompson FL, Sorokin A, Normand P, Dawyndt P et al. Ecological diversification in the Bacillus cereus Group. Environ Microbiol 2008; 10:851–865 [View Article][PubMed]
     [Google Scholar]
  28. Taylor RG, Walker DC, McInnes RR. E. coli host strains significantly affect the quality of small scale plasmid DNA preparations used for sequencing. Nucleic Acids Res 1993; 21:1677–1678 [View Article][PubMed]
     [Google Scholar]
  29. Gewain KM, Occi JL, Foor F, MacNeil DJ. Vectors for generating nested deletions and facilitating subcloning G+C-rich DNA between Escherichia coli and Streptomyces sp. Gene 1992; 119:149–150
     [Google Scholar]
  30. Gohar M, Gilois N, Graveline R, Garreau C, Sanchis V et al. A comparative study of Bacillus cereus, Bacillus thuringiensis and Bacillus anthracis extracellular proteomes. Proteomics 2005; 5:3696–3711 [View Article][PubMed]
     [Google Scholar]
  31. Perchat S, Dubois T, Zouhir S, Gominet M, Poncet S et al. A cell-cell communication system regulates protease production during sporulation in bacteria of the Bacillus cereus group. Mol Microbiol 2011; 82:619–633 [View Article][PubMed]
     [Google Scholar]
  32. Sali A, Blundell TL. Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol 1993; 234:779–815 [View Article][PubMed]
     [Google Scholar]
  33. Chen VB, Arendall WB, Headd JJ, Keedy DA, Immormino RM et al. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 2010; 66:12–21 [View Article][PubMed]
     [Google Scholar]
  34. Lereclus D, Agaisse H, Gominet M, Salamitou S, Sanchis V. Identification of a Bacillus thuringiensis gene that positively regulates transcription of the phosphatidylinositol-specific phospholipase C gene at the onset of the stationary phase. J Bacteriol 1996; 178:2749–2756 [View Article][PubMed]
     [Google Scholar]
  35. Duport C, Jobin M, Schmitt P. Adaptation in Bacillus cereus: from stress to disease. Front Microbiol 2016; 7:1550 [View Article][PubMed]
     [Google Scholar]
  36. Lereclus D, Vallade M, Chaufaux J, Arantes O, Rambaud S. Expansion of insecticidal host range of Bacillus thuringiensis by in vivo genetic recombination. Biotechnology 1992; 10:418–421 [View Article][PubMed]
     [Google Scholar]
  37. Agaisse H, Lereclus D. Structural and functional analysis of the promoter region involved in full expression of the cryIIIA toxin gene of Bacillus thuringiensis . Mol Microbiol 1994; 13:97–107 [View Article][PubMed]
     [Google Scholar]
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The signaling peptide PapR is required for the activity of the quorum-sensor PlcRa in Bacillus thuringiensis
Microbiology 166, 398 (2020); https://doi.org/10.1099/mic.0.000883
/content/journal/micro/10.1099/mic.0.000883
/content/journal/micro/10.1099/mic.0.000883
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