CerM and Its Antagonist CerN Are New Components of the Quorum Sensing System in Cereibacter sphaeroides, Signaling to the CckA/ChpT/CtrA System.

Jos�� Hern��ndez-Valle, Benjam��n Vega-Baray, Sebasti��n Poggio, Laura Camarena
Author Information
  1. Jos�� Hern��ndez-Valle: Departamento de Biolog��a Molecular y Biotecnolog��a, Instituto de Investigaciones Biom��dicas, Universidad Nacional Aut��noma de M��xico, Mexico City, Mexico. ORCID
  2. Benjam��n Vega-Baray: Departamento de Biolog��a Molecular y Biotecnolog��a, Instituto de Investigaciones Biom��dicas, Universidad Nacional Aut��noma de M��xico, Mexico City, Mexico. ORCID
  3. Sebasti��n Poggio: Departamento de Biolog��a Molecular y Biotecnolog��a, Instituto de Investigaciones Biom��dicas, Universidad Nacional Aut��noma de M��xico, Mexico City, Mexico. ORCID
  4. Laura Camarena: Departamento de Biolog��a Molecular y Biotecnolog��a, Instituto de Investigaciones Biom��dicas, Universidad Nacional Aut��noma de M��xico, Mexico City, Mexico. ORCID

Abstract

Cereibacter sphaeroides has a quorum sensing (QS) system that has been partially characterized. Using a bioinformatic approach, six LuxR homologs and one homolog of the acylhomoserine lactone synthase were identified in this bacterium, including the previously characterized CerR and CerI proteins. This study focused on determining the roles of two LuxR homologs, CerM and CerN. CerN lacks the HTH domain and, together with CerM, controls the expression of ctrA, which is part of the TCS CckA/ChpT/CtrA. CtrA is widely conserved in alpha-proteobacteria and regulates flagellar motility and other cellular processes. Genetic and biochemical data suggest that CerM indirectly represses ctrA expression, which is counteracted by its interaction with CerN-AHL. A transcriptomic study identified 181 genes regulated by CerM/CerN, with a conserved sequence in their regulatory regions likely indicating the CerM binding site. This hypothesis was supported by in vitro and in vivo DNA-protein interaction assays. Our results identified a transcription factor that could connect the QS system with the regulation of the two-component system CckA/ChpT/CtrA.

Keywords

References

  1. J Bacteriol. 2002 Dec;184(23):6515-21 [PMID: 12426339]
  2. BMC Microbiol. 2018 Oct 10;18(1):129 [PMID: 30305031]
  3. J Bacteriol. 1980 Nov;144(2):848-51 [PMID: 6253444]
  4. J Bacteriol. 1988 Jan;170(1):320-9 [PMID: 3257209]
  5. Annu Rev Microbiol. 2001;55:165-99 [PMID: 11544353]
  6. J Bacteriol. 2020 Mar 11;202(7): [PMID: 31932315]
  7. BMC Genomics. 2014 Feb 13;15:130 [PMID: 24524855]
  8. Proc Natl Acad Sci U S A. 1986 Nov;83(22):8447-51 [PMID: 3534890]
  9. J Bacteriol. 2007 Nov;189(22):8397-401 [PMID: 17890312]
  10. Curr Opin Microbiol. 2020 Jun;55:9-16 [PMID: 32045871]
  11. Mol Plant Microbe Interact. 2000 Dec;13(12):1283-92 [PMID: 11106020]
  12. PLoS Genet. 2020 Apr 23;16(4):e1008724 [PMID: 32324740]
  13. Nat Rev Mol Cell Biol. 2002 Sep;3(9):685-95 [PMID: 12209128]
  14. Proc Natl Acad Sci U S A. 1989 Sep;86(18):6973-7 [PMID: 2674941]
  15. Int J Mol Sci. 2013 Oct 15;14(10):20578-96 [PMID: 24132148]
  16. J Bacteriol. 2010 Jun;192(11):2701-10 [PMID: 20363938]
  17. J Bacteriol. 2002 Feb;184(4):913-8 [PMID: 11807050]
  18. J Bacteriol. 1998 Jun;180(11):2924-30 [PMID: 9603883]
  19. mBio. 2022 Aug 30;13(4):e0148122 [PMID: 35876508]
  20. J Bacteriol. 1992 Jan;174(1):245-53 [PMID: 1309519]
  21. Nat Commun. 2019 Feb 5;10(1):595 [PMID: 30723210]
  22. Microbiology (Reading). 2013 Jan;159(Pt 1):96-106 [PMID: 23154973]
  23. Nucleic Acids Res. 2015 Jul 1;43(W1):W39-49 [PMID: 25953851]
  24. Proc Natl Acad Sci U S A. 1979 Apr;76(4):1648-52 [PMID: 377280]
  25. Biomolecules. 2020 May 16;10(5): [PMID: 32429424]
  26. Annu Rev Microbiol. 1996;50:727-51 [PMID: 8905097]
  27. Gene. 1987;53(1):85-96 [PMID: 3596251]
  28. ISME J. 2010 Jan;4(1):61-77 [PMID: 19741735]
  29. Gene. 1993 May 15;127(1):15-21 [PMID: 8486283]
  30. Trends Plant Sci. 2013 Mar;18(3):167-74 [PMID: 23089307]
  31. J Bacteriol. 2015 Mar;197(5):833-47 [PMID: 25512309]
  32. Mol Microbiol. 1998 Jan;27(2):277-88 [PMID: 9484884]
  33. BMC Syst Biol. 2010 Apr 28;4:52 [PMID: 20426835]
  34. Curr Biol. 2008 Jul 22;18(14):1078-83 [PMID: 18639458]
  35. Biochemistry. 1981 Apr 28;20(9):2444-9 [PMID: 7236614]
  36. ISME J. 2008 Apr;2(4):345-9 [PMID: 18273067]
  37. J Bacteriol. 2000 Feb;182(3):805-11 [PMID: 10633117]
  38. J Bacteriol. 2013 Dec;195(23):5362-9 [PMID: 24078609]
  39. MicroPubl Biol. 2023 Jul 13;2023: [PMID: 37521139]
  40. Proc Natl Acad Sci U S A. 1998 Jan 6;95(1):120-5 [PMID: 9419339]
  41. J Bacteriol. 1997 Dec;179(23):7530-7 [PMID: 9393720]
  42. Microbiology (Reading). 2009 May;155(Pt 5):1669-1679 [PMID: 19372156]
  43. BMC Bioinformatics. 2013 Jan 16;14:4 [PMID: 23323735]
  44. Int J Mol Sci. 2021 Jun 09;22(12): [PMID: 34207734]
  45. J Bacteriol. 1997 Dec;179(24):7617-24 [PMID: 9401017]
  46. Gene. 1993 Jul 15;129(1):17-25 [PMID: 8335256]
  47. J Mol Biol. 1976 Jul 5;104(3):541-55 [PMID: 781293]
  48. Nature. 2002 Jun 27;417(6892):971-4 [PMID: 12087407]
  49. Mol Microbiol. 2012 Sep;85(5):916-33 [PMID: 22742196]
  50. Mol Microbiol. 2001 Apr;40(2):414-21 [PMID: 11309123]
  51. Front Microbiol. 2021 Jun 25;12:683109 [PMID: 34248901]
  52. Genome Biol. 2019 Nov 14;20(1):238 [PMID: 31727128]
  53. EMBO J. 2002 Sep 2;21(17):4393-401 [PMID: 12198141]
  54. J Gen Microbiol. 1962 Sep;28:607-16 [PMID: 13913485]
  55. Cell. 1996 Jan 12;84(1):83-93 [PMID: 8548829]
  56. Methods Enzymol. 2002;358:452-84 [PMID: 12474406]
  57. J Bacteriol. 2007 Apr;189(8):3208-16 [PMID: 17293429]
  58. PLoS One. 2014 Jan 08;9(1):e84831 [PMID: 24416296]
  59. Mol Microbiol. 2012 Nov;86(4):954-70 [PMID: 23035866]
  60. Chembiochem. 2005 Dec;6(12):2195-206 [PMID: 16283687]
  61. J Bacteriol. 2003 Dec;185(23):7001-7 [PMID: 14617666]
  62. Mol Microbiol. 2012 Feb;83(4):759-74 [PMID: 22211723]
  63. Nat Protoc. 2007;2(8):1849-61 [PMID: 17703195]
  64. Chem Rev. 2011 Jan 12;111(1):4-27 [PMID: 21142091]
  65. Gene. 1988 Oct 15;70(1):191-7 [PMID: 2853689]
  66. Nat Protoc. 2008;3(10):1578-88 [PMID: 18802439]
  67. Microbiology (Reading). 2015 Jan;161(Pt 1):50-56 [PMID: 25355937]
  68. Mol Microbiol. 2005 Nov;58(4):969-83 [PMID: 16262784]
  69. Int J Mol Sci. 2014 Jan 07;15(1):654-69 [PMID: 24402124]
  70. PLoS One. 2013 Jun 25;8(6):e66346 [PMID: 23825536]
  71. Environ Microbiol. 2019 Nov;21(11):4425-4445 [PMID: 31579997]
  72. Front Microbiol. 2019 Apr 12;10:803 [PMID: 31031742]
  73. Front Plant Sci. 2014 Jan 31;5:14 [PMID: 24550924]
  74. Mol Microbiol. 1998 Jan;27(2):289-97 [PMID: 9484885]
  75. J Bacteriol. 2005 Jun;187(11):3620-9 [PMID: 15901683]
  76. J Bacteriol. 2009 Dec;191(24):7402-9 [PMID: 19820098]
  77. Mol Plant Microbe Interact. 2017 Dec;30(12):1009-1019 [PMID: 28871850]
  78. ISME J. 2013 Dec;7(12):2274-86 [PMID: 23823498]

Grants

  1. /This study was supported by Direcci��n General de Asuntos del Personal Acad��mico, Universidad Nacional Aut��noma de M��xico (DGAPA-PAPIIT) grant IN215023 and CONAHCyT (CBF2023-2024-501), CONAHCyT fellowship (749450).

MeSH Term

Quorum Sensing
Gene Expression Regulation, Bacterial
Bacterial Proteins
Signal Transduction
Gene Expression Profiling
Trans-Activators
Protein Binding
Repressor Proteins
Transcription Factors

Chemicals

Bacterial Proteins
Trans-Activators
LuxR autoinducer binding proteins
Repressor Proteins
Transcription Factors

Word Cloud

Created with Highcharts 10.0.0CerMsystemLuxRidentifiedCerNCckA/ChpT/CtrACereibactersphaeroidesquorumsensingQScharacterizedhomologsCerIstudyexpressionctrACtrAconservedinteractionSystempartiallyUsingbioinformaticapproachsixonehomologacylhomoserinelactonesynthasebacteriumincludingpreviouslyCerRproteinsfocuseddeterminingrolestwolacksHTHdomaintogethercontrolspartTCSwidelyalpha-proteobacteriaregulatesflagellarmotilitycellularprocessesGeneticbiochemicaldatasuggestindirectlyrepressescounteractedCerN-AHLtranscriptomic181genesregulatedCerM/CerNsequenceregulatoryregionslikelyindicatingbindingsitehypothesissupportedvitrovivoDNA-proteinassaysresultstranscriptionfactorconnectregulationtwo-componentAntagonistNewComponentsQuorumSensingSignalingCckATrlRtwo���component

Similar Articles

Cited By

No available data.