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Volume 169, Issue 2

Cross-species activation of hydrogen cyanide production by a promiscuous quorum-sensing receptor promotes competition in a dual-species model Open Access

Abstract

Many saprophytic bacteria have LuxR-I-type acyl-homoserine lactone (AHL) quorum-sensing systems that may be important for competing with other bacteria in complex soil communities. LuxR AHL receptors specifically interact with cognate AHLs to cause changes in expression of target genes. Some LuxR-type AHL receptors have relaxed specificity and are responsive to non-cognate AHLs. These promiscuous receptors might be used to sense and respond to AHLs produced by other bacteria by eavesdropping. We are interested in understanding the role of eavesdropping during interspecies competition. The soil saprophyte has a single AHL circuit, CviR-I, which produces and responds to hexanoyl-HSL (C6-HSL). The AHL receptor CviR can respond to a variety of AHLs in addition to C6-HSL. In prior studies we have utilized a coculture model with and another soil saprophyte, . Using this model, we previously showed that promiscuous activation of CviR by AHLs provides a competitive advantage to . Here, we show that AHLs activate transcription of dozens of genes in including the genes coding for production of hydrogen cyanide. We show that hydrogen cyanide production is population density-dependent and demonstrate that the cross-induction of hydrogen cyanide by AHLs provides a competitive advantage to . Our results provide new information on quorum sensing and are the basis for future studies aimed at understanding the role of eavesdropping in interspecies competition.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): antibiotic , Chromobacterium , coculture , competition , cyanide and quorum sensing
Funding
This study was supported by the:
  • National Institute of General Medical Sciences (Award P20GM113117)
    • Principle Award Recipient: NotApplicable
  • National Institute of General Medical Sciences (Award P20GM103638)
    • Principle Award Recipient: NotApplicable
  • National Institute of General Medical Sciences (Award P20GM103418)
    • Principle Award Recipient: SaidaBenomar
  • National Institute of General Medical Sciences (Award T32 GM08545)
    • Principle Award Recipient: KaraC Evans
  • National Institute of General Medical Sciences (Award R35GM133572)
    • Principle Award Recipient: JosephineR Chandler
© 2023 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
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2023-02-15
2024-05-04
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References

  1. Hawver LA, Jung SA, Ng WL. Specificity and complexity in bacterial quorum-sensing systems. FEMS Microbiol Rev 2016; 40:738–752 [View Article] [PubMed]
     [Google Scholar]
  2. McClean KH, Winson MK, Fish L, Taylor A, Chhabra SR et al. Quorum sensing and Chromobacterium violaceum: exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones. Microbiology 1997; 143 (Pt 12):3703–3711 [View Article]
     [Google Scholar]
  3. Swem LR, Swem DL, O’Loughlin CT, Gatmaitan R, Zhao B et al. A quorum-sensing antagonist targets both membrane-bound and cytoplasmic receptors and controls bacterial pathogenicity. Mol Cell 2009; 35:143–153 [View Article] [PubMed]
     [Google Scholar]
  4. Abisado RG, Benomar S, Klaus JR, Dandekar AA, Chandler JR. Bacterial quorum sensing and microbial community interactions. mBio 2018; 9:e02331-17 [View Article]
     [Google Scholar]
  5. Chandler JR, Heilmann S, Mittler JE, Greenberg EP. Acyl-homoserine lactone-dependent eavesdropping promotes competition in a laboratory co-culture model. ISME J 2012; 6:2219–2228 [View Article] [PubMed]
     [Google Scholar]
  6. Seyedsayamdost MR, Chandler JR, Blodgett JAV, Lima PS, Duerkop BA et al. Quorum-sensing-regulated bactobolin production by Burkholderia thailandensis E264. Org Lett 2010; 12:716–719 [View Article] [PubMed]
     [Google Scholar]
  7. Duerkop BA, Varga J, Chandler JR, Peterson SB, Herman JP et al. Quorum-sensing control of antibiotic synthesis in Burkholderia thailandensis. J Bacteriol 2009; 191:3909–3918 [View Article] [PubMed]
     [Google Scholar]
  8. Chandler JR, Duerkop BA, Hinz A, West TE, Herman JP et al. Mutational analysis of Burkholderia thailandensis quorum sensing and self-aggregation. J Bacteriol 2009; 191:5901–5909 [View Article] [PubMed]
     [Google Scholar]
  9. Brett PJ, DeShazer D, Woods DE. Burkholderia thailandensis sp. nov., a Burkholderia pseudomallei-like species. Int J Syst Bacteriol 1998; 48 Pt 1:317–320 [View Article]
     [Google Scholar]
  10. Rietsch A, Vallet-Gely I, Dove SL, Mekalanos JJ. ExsE, a secreted regulator of type III secretion genes in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 2005; 102:8006–8011 [View Article] [PubMed]
     [Google Scholar]
  11. Spaink HP, Okker RJ, Wijffelman CA, Pees E, Lugtenberg BJ. Promoters in the nodulation region of the Rhizobium leguminosarum Sym plasmid pRL1JI. Plant Mol Biol 1987; 9:27–39 [View Article]
     [Google Scholar]
  12. Liao Y, Smyth GK, Shi W. The R package Rsubread is easier, faster, cheaper and better for alignment and quantification of RNA sequencing reads. Nucleic Acids Res 2019; 47:e47 [View Article]
     [Google Scholar]
  13. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010; 26:139–140 [View Article]
     [Google Scholar]
  14. Santana-Garcia W, Castro-Mondragon JA, Padilla-Gálvez M, Nguyen NTT, Elizondo-Salas A et al. RSAT 2022: regulatory sequence analysis tools. Nucleic Acids Res 2022; 50:W670–6 [View Article]
     [Google Scholar]
  15. Lu Z, Berry K, Hu Z, Zhan Y, Ahn T-H et al. TSSr: an R package for comprehensive analyses of TSS sequencing data. NAR Genom Bioinform 2021; 3:lqab108 [View Article]
     [Google Scholar]
  16. Majerczyk C, Brittnacher M, Jacobs M, Armour CD, Radey M et al. Global analysis of the Burkholderia thailandensis quorum sensing-controlled regulon. J Bacteriol 2014; 196:1412–1424 [View Article] [PubMed]
     [Google Scholar]
  17. Short SM, van Tol S, MacLeod HJ, Dimopoulos G. Hydrogen cyanide produced by the soil bacterium Chromobacterium sp. Panama contributes to mortality in Anopheles gambiae mosquito larvae. Sci Rep 2018; 8:8358 [View Article]
     [Google Scholar]
  18. Mun W, Kwon H, Im H, Choi SY, Monnappa AK et al. Cyanide production by Chromobacterium piscinae shields it from Bdellovibrio bacteriovorus HD100 predation. mBio 2017
     [Google Scholar]
  19. Smalley NE, An D, Parsek MR, Chandler JR, Dandekar AA. Quorum sensing protects Pseudomonas aeruginosa against cheating by other species in a laboratory coculture model. J Bacteriol 2015; 197:3154–3159 [View Article]
     [Google Scholar]
  20. Gilchrist FJ, Alcock A, Belcher J, Brady M, Jones A et al. Variation in hydrogen cyanide production between different strains of Pseudomonas aeruginosa. Eur Respir J 2011; 38:409–414 [View Article] [PubMed]
     [Google Scholar]
  21. Chen G, Swem LR, Swem DL, Stauff DL, O’Loughlin CT et al. A strategy for antagonizing quorum sensing. Mol Cell 2011; 42:199–209 [View Article] [PubMed]
     [Google Scholar]
  22. Stauff DL, Bassler BL. Quorum sensing in Chromobacterium violaceum: DNA recognition and gene regulation by the CviR receptor. J Bacteriol 2011; 193:3871–3878 [View Article] [PubMed]
     [Google Scholar]
  23. Valente RS, Nadal-Jimenez P, Carvalho AFP, Vieira FJD, Xavier KB. Signal integration in quorum sensing enables cross-species induction of virulence in Pectobacterium wasabiae. mBio 2017; 8:e00398-17 [View Article]
     [Google Scholar]
  24. Hosni T, Moretti C, Devescovi G, Suarez-Moreno ZR, Fatmi MB et al. Sharing of quorum-sensing signals and role of interspecies communities in a bacterial plant disease. ISME J 2011; 5:1857–1870 [View Article] [PubMed]
     [Google Scholar]
  25. Dulla GFJ, Lindow SE. Acyl-homoserine lactone-mediated cross talk among epiphytic bacteria modulates behavior of Pseudomonas syringae on leaves. ISME J 2009; 3:825–834 [View Article] [PubMed]
     [Google Scholar]
  26. Riedel K, Hentzer M, Geisenberger O, Huber B, Steidle A et al. N-acylhomoserine-lactone-mediated communication between Pseudomonas aeruginosa and Burkholderia cepacia in mixed biofilms. Microbiology 2001; 147:3249–3262 [View Article]
     [Google Scholar]
  27. Wellington S, Greenberg EP. Quorum sensing signal selectivity and the potential for interspecies cross talk. mBio 2019; 10:e00146-19 [View Article]
     [Google Scholar]
  28. Collins CH, Arnold FH, Leadbetter JR. Directed evolution of Vibrio fischeri LuxR for increased sensitivity to a broad spectrum of acyl-homoserine lactones. Mol Microbiol 2005; 55:712–723 [View Article] [PubMed]
     [Google Scholar]
  29. Hawkins AC, Arnold FH, Stuermer R, Hauer B, Leadbetter JR. Directed evolution of Vibrio fischeri LuxR for improved response to butanoyl-homoserine lactone. Appl Environ Microbiol 2007; 73:5775–5781 [View Article] [PubMed]
     [Google Scholar]
  30. Lintz MJ, Oinuma K, Wysoczynski CL, Greenberg EP, Churchill MEA. Crystal structure of QscR, a Pseudomonas aeruginosa quorum sensing signal receptor. Proc Natl Acad Sci 2011; 108:15763–15768 [View Article]
     [Google Scholar]
  31. Lozano GL, Guan C, Cao Y, Borlee BR, Broderick NA et al. A chemical counterpunch: Chromobacterium violaceum ATCC 31532 produces violacein in response to translation-inhibiting antibiotics. mBio 2020; 11:e00948-20 [View Article]
     [Google Scholar]
  32. Wang M, Schaefer AL, Dandekar AA, Greenberg EP. Quorum sensing and policing of Pseudomonas aeruginosa social cheaters. Proc Natl Acad Sci 2015; 112:2187–2191 [View Article]
     [Google Scholar]
  33. Schuster M, Urbanowski ML, Greenberg EP. Promoter specificity in Pseudomonas aeruginosa quorum sensing revealed by DNA binding of purified LasR. Proc Natl Acad Sci 2004; 101:15833–15839 [View Article]
     [Google Scholar]
  34. Pessi G, Haas D. Transcriptional control of the hydrogen cyanide biosynthetic genes hcnABC by the anaerobic regulator ANR and the quorum-sensing regulators LasR and RhlR in Pseudomonas aeruginosa. J Bacteriol 2000; 182:6940–6949 [View Article] [PubMed]
     [Google Scholar]
  35. López CM, Rholl DA, Trunck LA, Schweizer HP. Versatile dual-technology system for markerless allele replacement in Burkholderia pseudomallei. Appl Environ Microbiol 2009; 75:6496–6503 [View Article] [PubMed]
     [Google Scholar]
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Cross-species activation of hydrogen cyanide production by a promiscuous quorum-sensing receptor promotes Chromobacterium subtsugae competition in a dual-species model
Microbiology 169, 001294 (2023); https://doi.org/10.1099/mic.0.001294
/content/journal/micro/10.1099/mic.0.001294
/content/journal/micro/10.1099/mic.0.001294
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