#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Quadruple Quorum-Sensing Inputs Control Virulence and Maintain System Robustness


Quorum-sensing (QS) is a microbial cell-cell communication process that allows bacteria to function as a collective group. Many pathogens, including Vibrio cholerae, the causative agent of cholera, depend on QS to regulate important cellular processes that are essential for survival and adaptation inside and outside of their hosts. Since its discovery, the V. cholerae QS system has served as a model to understand how bacterial pathogens employ QS for temporal control of virulence factor production. Yet, after a decade of research, our understanding of the V. cholerae QS system is still incomplete. Here we re-define the QS network architecture of this important pathogen. We show that two novel sensory inputs function in parallel with the two canonical QS pathways to regulate V. cholerae virulence gene expression. Moreover, our study illustrates a strategy that bacteria employ to maintain QS system robustness. By perceiving multiple parallel sensory inputs, the V. cholerae QS network is structured to be highly resistant to signal perturbations, therefore preventing premature commitment to QS. Our study provides new insights into how bacterial pathogens integrate multiple sensory signals to elicit robust and coordinated QS responses.


Vyšlo v časopise: Quadruple Quorum-Sensing Inputs Control Virulence and Maintain System Robustness. PLoS Pathog 11(4): e32767. doi:10.1371/journal.ppat.1004837
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004837

Souhrn

Quorum-sensing (QS) is a microbial cell-cell communication process that allows bacteria to function as a collective group. Many pathogens, including Vibrio cholerae, the causative agent of cholera, depend on QS to regulate important cellular processes that are essential for survival and adaptation inside and outside of their hosts. Since its discovery, the V. cholerae QS system has served as a model to understand how bacterial pathogens employ QS for temporal control of virulence factor production. Yet, after a decade of research, our understanding of the V. cholerae QS system is still incomplete. Here we re-define the QS network architecture of this important pathogen. We show that two novel sensory inputs function in parallel with the two canonical QS pathways to regulate V. cholerae virulence gene expression. Moreover, our study illustrates a strategy that bacteria employ to maintain QS system robustness. By perceiving multiple parallel sensory inputs, the V. cholerae QS network is structured to be highly resistant to signal perturbations, therefore preventing premature commitment to QS. Our study provides new insights into how bacterial pathogens integrate multiple sensory signals to elicit robust and coordinated QS responses.


Zdroje

1. Williams P, Winzer K, Chan WC, Camara M. Look who's talking: communication and quorum sensing in the bacterial world. Philos Trans R Soc Lond B Biol Sci. 2007;362(1483): 1119–1134. 17360280

2. Novick RP, Geisinger E. Quorum sensing in staphylococci. Annu Rev Genet. 2008;42: 541–564. doi: 10.1146/annurev.genet.42.110807.091640 18713030

3. Ng WL, Bassler BL. Bacterial Quorum-Sensing Network Architectures. Annu Rev Genet. 2009;43: 197–222. doi: 10.1146/annurev-genet-102108-134304 19686078

4. Rutherford ST, Bassler BL. Bacterial quorum sensing: its role in virulence and possibilities for its control. Cold Spring Harb Perspect Med. 2012;2(11): a012427. doi: 10.1101/cshperspect.a012427 23125205

5. Schuster M, Sexton DJ, Diggle SP, Greenberg EP. Acyl-homoserine lactone quorum sensing: from evolution to application. Annu Rev Microbiol. 2013;67: 43–63. doi: 10.1146/annurev-micro-092412-155635 23682605

6. Miller MB, Skorupski K, Lenz DH, Taylor RK, Bassler BL. Parallel quorum sensing systems converge to regulate virulence in Vibrio cholerae. Cell. 2002;110(3): 303–314. 12176318

7. Zhu J, Miller MB, Vance RE, Dziejman M, Bassler BL, Mekalanos JJ. Quorum-sensing regulators control virulence gene expression in Vibrio cholerae. Proc Natl Acad Sci U S A. 2002;99(5): 3129–3134. 11854465

8. Hammer BK, Bassler BL. Quorum sensing controls biofilm formation in Vibrio cholerae. Mol Microbiol. 2003;50(1): 101–104. 14507367

9. Zhu J, Mekalanos JJ. Quorum sensing-dependent biofilms enhance colonization in Vibrio cholerae. Dev Cell. 2003;5(4): 647–656. 14536065

10. Joelsson A, Kan B, Zhu J. Quorum sensing enhances the stress response in Vibrio cholerae. Appl Environ Microbiol. 2007;73(11): 3742–3746. 17434996

11. Tsou AM, Zhu J. Quorum sensing negatively regulates hemolysin transcriptionally and posttranslationally in Vibrio cholerae. Infect Immun. 2010;78(1): 461–467. doi: 10.1128/IAI.00590-09 19858311

12. Zheng J, Shin OS, Cameron DE, Mekalanos JJ. Quorum sensing and a global regulator TsrA control expression of type VI secretion and virulence in Vibrio cholerae. Proc Natl Acad Sci U S A. 2010;107(49): 21128–21133. doi: 10.1073/pnas.1014998107 21084635

13. Antonova ES, Hammer BK. Quorum-sensing autoinducer molecules produced by members of a multispecies biofilm promote horizontal gene transfer to Vibrio cholerae. FEMS Microbiol Lett. 2011;322(1): 68–76. doi: 10.1111/j.1574-6968.2011.02328.x 21658103

14. Suckow G, Seitz P, Blokesch M. Quorum sensing contributes to natural transformation of Vibrio cholerae in a species-specific manner. J Bacteriol. 2011;193(18): 4914–4924. doi: 10.1128/JB.05396-11 21784943

15. Blokesch M. A quorum sensing-mediated switch contributes to natural transformation of Vibrio cholerae. Mob Genet Elements. 2012;2(5): 224–227. 23446800

16. Lo Scrudato M, Blokesch M. The regulatory network of natural competence and transformation of Vibrio cholerae. PLoS Genet. 2012;8(6): e1002778. doi: 10.1371/journal.pgen.1002778 22737089

17. Shao Y, Bassler BL. Quorum regulatory small RNAs repress type VI secretion in Vibrio cholerae. Mol Microbiol. 2014;92(5): 921–930. doi: 10.1111/mmi.12599 24698180

18. Henke JM, Bassler BL. Three parallel quorum-sensing systems regulate gene expression in Vibrio harveyi. J Bacteriol. 2004;186(20): 6902–6914. 15466044

19. Jahan N, Potter JA, Sheikh MA, Botting CH, Shirran SL, Westwood NJ, et al. Insights into the biosynthesis of the Vibrio cholerae major autoinducer CAI-1 from the crystal structure of the PLP-dependent enzyme CqsA. J Mol Biol. 2009;392(3): 763–773. doi: 10.1016/j.jmb.2009.07.042 19631226

20. Kelly RC, Bolitho ME, Higgins DA, Lu W, Ng WL, Jeffrey PD, et al. The Vibrio cholerae quorum-sensing autoinducer CAI-1: analysis of the biosynthetic enzyme CqsA. Nat Chem Biol. 2009;5(12): 891–895. doi: 10.1038/nchembio.237 19838203

21. Ng WL, Perez LJ, Wei Y, Kraml C, Semmelhack MF, Bassler BL. Signal production and detection specificity in Vibrio CqsA/CqsS quorum-sensing systems. Mol Microbiol. 2011;79(6): 1407–1417. doi: 10.1111/j.1365-2958.2011.07548.x 21219472

22. Wei Y, Perez LJ, Ng WL, Semmelhack MF, Bassler BL. Mechanism of Vibrio cholerae Autoinducer-1 Biosynthesis. ACS Chem Biol. 2011;6(4): 356–365. doi: 10.1021/cb1003652 21197957

23. Higgins DA, Pomianek ME, Kraml CM, Taylor RK, Semmelhack MF, Bassler BL. The major Vibrio cholerae autoinducer and its role in virulence factor production. Nature. 2007;450(7171): 883–886. 18004304

24. Surette MG, Miller MB, Bassler BL. Quorum sensing in Escherichia coli, Salmonella typhimurium, and Vibrio harveyi: a new family of genes responsible for autoinducer production. Proc Natl Acad Sci U S A. 1999;96(4): 1639–1644. 9990077

25. Chen X, Schauder S, Potier N, Van Dorsselaer A, Pelczer I, Bassler BL, et al. Structural identification of a bacterial quorum-sensing signal containing boron. Nature. 2002;415(6871): 545–549. 11823863

26. Pereira CS, Thompson JA, Xavier KB. AI-2-mediated signalling in bacteria. FEMS Microbiol Rev. 2013;37(2): 156–181. doi: 10.1111/j.1574-6976.2012.00345.x 22712853

27. Bassler BL, Wright M, Silverman MR. Multiple signalling systems controlling expression of luminescence in Vibrio harveyi: sequence and function of genes encoding a second sensory pathway. Mol Microbiol. 1994;13(2): 273–286. 7984107

28. Lenz DH, Mok KC, Lilley BN, Kulkarni RV, Wingreen NS, Bassler BL. The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae. Cell. 2004;118(1): 69–82. 15242645

29. Rutherford ST, van Kessel JC, Shao Y, Bassler BL. AphA and LuxR/HapR reciprocally control quorum sensing in vibrios. Genes Dev. 2011;25(4): 397–408. doi: 10.1101/gad.2015011 21325136

30. Shao Y, Bassler BL. Quorum-sensing non-coding small RNAs use unique pairing regions to differentially control mRNA targets. Mol Microbiol. 2012;83(3): 599–611. doi: 10.1111/j.1365-2958.2011.07959.x 22229925

31. Lenz DH, Miller MB, Zhu J, Kulkarni RV, Bassler BL. CsrA and three redundant small RNAs regulate quorum sensing in Vibrio cholerae. Mol Microbiol. 2005;58(4): 1186–1202. 16262799

32. Shikuma NJ, Fong JC, Odell LS, Perchuk BS, Laub MT, Yildiz FH. Overexpression of VpsS, a hybrid sensor kinase, enhances biofilm formation in Vibrio cholerae. J Bacteriol. 2009;191(16): 5147–5158. doi: 10.1128/JB.00401-09 19525342

33. Wei Y, Ng WL, Cong J, Bassler BL. Ligand and antagonist driven regulation of the Vibrio cholerae quorum-sensing receptor CqsS. Mol Microbiol. 2012;83(6): 1095–1108. doi: 10.1111/j.1365-2958.2012.07992.x 22295878

34. Fu Y, Waldor MK, Mekalanos JJ. Tn-Seq analysis of Vibrio cholerae intestinal colonization reveals a role for T6SS-mediated antibacterial activity in the host. Cell Host Microbe. 2013;14(6): 652–663. doi: 10.1016/j.chom.2013.11.001 24331463

35. Kamp HD, Patimalla-Dipali B, Lazinski DW, Wallace-Gadsden F, Camilli A. Gene fitness landscapes of Vibrio cholerae at important stages of its life cycle. PLoS Pathog. 2013;9(12): e1003800. doi: 10.1371/journal.ppat.1003800 24385900

36. Hammer BK, Bassler BL. Regulatory small RNAs circumvent the conventional quorum sensing pathway in pandemic Vibrio cholerae. Proc Natl Acad Sci U S A. 2007;104(27): 11145–11149. 17556542

37. Perego M, Cole SP, Burbulys D, Trach K, Hoch JA. Characterization of the gene for a protein kinase which phosphorylates the sporulation-regulatory proteins Spo0A and Spo0F of Bacillus subtilis. J Bacteriol. 1989;171(11): 6187–6196. 2509430

38. Trach KA, Hoch JA. Multisensory activation of the phosphorelay initiating sporulation in Bacillus subtilis: identification and sequence of the protein kinase of the alternate pathway. Mol Microbiol. 1993;8(1): 69–79. 8497199

39. LeDeaux JR, Grossman AD. Isolation and characterization of kinC, a gene that encodes a sensor kinase homologous to the sporulation sensor kinases KinA and KinB in Bacillus subtilis. J Bacteriol. 1995;177(1): 166–175. 8002614

40. Jiang M, Shao W, Perego M, Hoch JA. Multiple histidine kinases regulate entry into stationary phase and sporulation in Bacillus subtilis. Mol Microbiol. 2000;38(3): 535–542. 11069677

41. LeDeaux JR, Yu N, Grossman AD. Different roles for KinA, KinB, and KinC in the initiation of sporulation in Bacillus subtilis. J Bacteriol. 1995;177(3): 861–863. 7836330

42. Laub MT, Goulian M. Specificity in two-component signal transduction pathways. Annu Rev Genet. 2007;41: 121–145. 18076326

43. Cornforth DM, Popat R, McNally L, Gurney J, Scott-Phillips TC, Ivens A, et al. Combinatorial quorum sensing allows bacteria to resolve their social and physical environment. Proc Natl Acad Sci U S A. 2014;111(11): 4280–4284. doi: 10.1073/pnas.1319175111 24594597

44. Drees B, Reiger M, Jung K, Bischofs IB. A modular view of the diversity of cell-density-encoding schemes in bacterial quorum-sensing systems. Biophys J. 2014;107(1): 266–277. doi: 10.1016/j.bpj.2014.05.031 24988360

45. Ng WL, Perez L, Cong J, Semmelhack MF, Bassler BL. Broad spectrum pro-quorum-sensing molecules as inhibitors of virulence in vibrios. PLoS Pathog. 2012;8(6): e1002767. doi: 10.1371/journal.ppat.1002767 22761573

46. Mok KC, Wingreen NS, Bassler BL. Vibrio harveyi quorum sensing: a coincidence detector for two autoinducers controls gene expression. Embo J. 2003;22(4): 870–881. 12574123

47. Bari SM, Roky MK, Mohiuddin M, Kamruzzaman M, Mekalanos JJ, Faruque SM. Quorum-sensing autoinducers resuscitate dormant Vibrio cholerae in environmental water samples. Proc Natl Acad Sci U S A. 2013;110(24): 9926–9931. doi: 10.1073/pnas.1307697110 23716683

48. Federle MJ, Bassler BL. Interspecies communication in bacteria. J Clin Invest. 2003;112(9): 1291–1299. 14597753

49. Borziak K, Zhulin IB. FIST: a sensory domain for diverse signal transduction pathways in prokaryotes and ubiquitin signaling in eukaryotes. Bioinformatics. 2007;23(19): 2518–2521. 17855421

50. Anantharaman V, Aravind L. Cache—a signaling domain common to animal Ca(2+)-channel subunits and a class of prokaryotic chemotaxis receptors. Trends Biochem Sci. 2000;25(11): 535–537. 11084361

51. Chen Y, Cao S, Chai Y, Clardy J, Kolter R, Guo JH, et al. A Bacillus subtilis sensor kinase involved in triggering biofilm formation on the roots of tomato plants. Mol Microbiol. 2012;85(3): 418–430. doi: 10.1111/j.1365-2958.2012.08109.x 22716461

52. Shemesh M, Chai Y. A combination of glycerol and manganese promotes biofilm formation in Bacillus subtilis via histidine kinase KinD signaling. J Bacteriol. 2013;195(12): 2747–2754. doi: 10.1128/JB.00028-13 23564171

53. Thelin KH, Taylor RK. Toxin-coregulated pilus, but not mannose-sensitive hemagglutinin, is required for colonization by Vibrio cholerae O1 El Tor biotype and O139 strains. Infect Immun. 1996;64(7): 2853–2856. 8698524

54. Skorupski K, Taylor RK. Positive selection vectors for allelic exchange. Gene. 1996;169(1): 47–52. 8635748

55. Svenningsen SL, Waters CM, Bassler BL. A negative feedback loop involving small RNAs accelerates Vibrio cholerae's transition out of quorum-sensing mode. Genes Dev. 2008;22(2): 226–238. doi: 10.1101/gad.1629908 18198339

Štítky
Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

Článok vyšiel v časopise

PLOS Pathogens


2015 Číslo 4
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#