1887

Abstract

The signalling molecule bis-(3′–5′)-cyclic-dimeric guanosine monophosphate (c-di-GMP) is a central regulator of diverse cellular functions, including motility, biofilm formation, cell cycle progression and virulence, in bacteria. Multiple diguanylate cyclase and phosphodiesterase-domain-containing proteins (GGDEF and EAL/HD-GYP, respectively) modulate the levels of the second messenger c-di-GMP to transmit signals and obtain such specific cellular responses. In the genus this c-di-GMP network is poorly studied. In this work, we evaluated the expression of two phenotypes in regulated by c-di-GMP, biofilm formation and motility, under the influence of ectopic expression of proteins with EAL or GGDEF domains that regulates the c-di-GMP level. In agreement with previous reports for other bacteria, we observed that is able to form biofilm and reduce its motility only when GGDEF domain protein is expressed. Moreover we identify a GGDEF domain protein (BB3576) with diguanylate cyclase activity that participates in motility and biofilm regulation in . These results demonstrate for the first time, to our knowledge, the presence of c-di-GMP regulatory signalling in .

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2013-05-01
2019-10-15
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References

  1. Akerley B. J. , Miller J. F. . ( 1993; ). Flagellin gene transcription in Bordetella bronchiseptica is regulated by the BvgAS virulence control system. . J Bacteriol 175:, 3468–3479.[PubMed]
    [Google Scholar]
  2. Akerley B. J. , Monack D. M. , Falkow S. , Miller J. F. . ( 1992; ). The bvgAS locus negatively controls motility and synthesis of flagella in Bordetella bronchiseptica . . J Bacteriol 174:, 980–990.[PubMed]
    [Google Scholar]
  3. Amarasinghe J. J. , D’Hondt R. E. , Waters C. M. , Mantis N. J. . ( 2013; ). Exposure of Salmonella enterica Serovar Typhimurium to a protective monoclonal IgA triggers exopolysaccharide production via a diguanylate cyclase-dependent pathway. . Infect Immun 81:, 653–664. [CrossRef] [PubMed]
    [Google Scholar]
  4. Amikam D. , Galperin M. Y. . ( 2006; ). PilZ domain is part of the bacterial c-di-GMP binding protein. . Bioinformatics 22:, 3–6. [CrossRef] [PubMed]
    [Google Scholar]
  5. Anantharaman V. , Aravind L. . ( 2000; ). Cache – a signaling domain common to animal Ca2+-channel subunits and a class of prokaryotic chemotaxis receptors. . Trends Biochem Sci 25:, 535–537. [CrossRef] [PubMed]
    [Google Scholar]
  6. Conover M. S. , Mishra M. , Deora R. . ( 2011; ). Extracellular DNA is essential for maintaining Bordetella biofilm integrity on abiotic surfaces and in the upper respiratory tract of mice. . PLoS ONE 6:, e16861. [CrossRef] [PubMed]
    [Google Scholar]
  7. Cotter P. A. , Miller J. F. . ( 1997; ). A mutation in the Bordetella bronchiseptica bvgS gene results in reduced virulence and increased resistance to starvation, and identifies a new class of Bvg-regulated antigens. . Mol Microbiol 24:, 671–685. [CrossRef] [PubMed]
    [Google Scholar]
  8. Dombrecht B. , Vanderleyden J. , Michiels J. . ( 2001; ). Stable RK2-derived cloning vectors for the analysis of gene expression and gene function in Gram-negative bacteria. . Mol Plant Microbe Interact 14:, 426–430. [CrossRef] [PubMed]
    [Google Scholar]
  9. Fernández J. , Sisti F. , Bottero D. , Gaillard M. E. , Hozbor D. . ( 2005; ). Constitutive expression of bvgR-repressed factors is not detrimental to the Bordetella bronchiseptica–host interaction. . Res Microbiol 156:, 843–850. [CrossRef] [PubMed]
    [Google Scholar]
  10. Galperin M. Y. . ( 2004; ). Bacterial signal transduction network in a genomic perspective. . Environ Microbiol 6:, 552–567. [CrossRef] [PubMed]
    [Google Scholar]
  11. Galperin M. Y. . ( 2005; ). A census of membrane-bound and intracellular signal transduction proteins in bacteria: bacterial IQ, extroverts and introverts. . BMC Microbiol 5:, 35. [CrossRef] [PubMed]
    [Google Scholar]
  12. Galperin M. Y. . ( 2006; ). Structural classification of bacterial response regulators: diversity of output domains and domain combinations. . J Bacteriol 188:, 4169–4182. [CrossRef] [PubMed]
    [Google Scholar]
  13. Galperin M. Y. , Nikolskaya A. N. , Koonin E. V. . ( 2001; ). Novel domains of the prokaryotic two-component signal transduction systems. . FEMS Microbiol Lett 203:, 11–21. [CrossRef] [PubMed]
    [Google Scholar]
  14. Goodnow R. A. . ( 1980; ). Biology of Bordetella bronchiseptica . . Microbiol Rev 44:, 722–738.[PubMed]
    [Google Scholar]
  15. Harvill E. T. , Cotter P. A. , Yuk M. H. , Miller J. F. . ( 1999; ). Probing the function of Bordetella bronchiseptica adenylate cyclase toxin by manipulating host immunity. . Infect Immun 67:, 1493–1500.[PubMed]
    [Google Scholar]
  16. Harvill E. T. , Preston A. , Cotter P. A. , Allen A. G. , Maskell D. J. , Miller J. F. . ( 2000; ). Multiple roles for Bordetella lipopolysaccharide molecules during respiratory tract infection. . Infect Immun 68:, 6720–6728. [CrossRef] [PubMed]
    [Google Scholar]
  17. Hengge R. . ( 2009; ). Principles of c-di-GMP signalling in bacteria. . Nat Rev Microbiol 7:, 263–273. [CrossRef] [PubMed]
    [Google Scholar]
  18. Inatsuka C. S. , Xu Q. , Vujkovic-Cvijin I. , Wong S. , Stibitz S. , Miller J. F. , Cotter P. A. . ( 2010; ). Pertactin is required for Bordetella species to resist neutrophil-mediated clearance. . Infect Immun 78:, 2901–2909. [CrossRef] [PubMed]
    [Google Scholar]
  19. Irie Y. , Mattoo S. , Yuk M. H. . ( 2004; ). The Bvg virulence control system regulates biofilm formation in Bordetella bronchiseptica . . J Bacteriol 186:, 5692–5698. [CrossRef] [PubMed]
    [Google Scholar]
  20. Jenal U. , Malone J. . ( 2006; ). Mechanisms of cyclic-di-GMP signaling in bacteria. . Annu Rev Genet 40:, 385–407. [CrossRef] [PubMed]
    [Google Scholar]
  21. Kolter R. , Greenberg E. P. . ( 2006; ). Microbial sciences: the superficial life of microbes. . Nature 441:, 300–302. [CrossRef] [PubMed]
    [Google Scholar]
  22. Kovach M. E. , Elzer P. H. , Hill D. S. , Robertson G. T. , Farris M. A. , Roop R. M. II , Peterson K. M. . ( 1995; ). Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. . Gene 166:, 175–176. [CrossRef] [PubMed]
    [Google Scholar]
  23. Kulesekara H. , Lee V. , Brencic A. , Liberati N. , Urbach J. , Miyata S. , Lee D. G. , Neely A. N. , Hyodo M. et al. ( 2006; ). Analysis of Pseudomonas aeruginosa diguanylate cyclases and phosphodiesterases reveals a role for bis-(3′–5′)-cyclic-GMP in virulence. . Proc Natl Acad Sci U S A 103:, 2839–2844. [CrossRef] [PubMed]
    [Google Scholar]
  24. Lai T. H. , Kumagai Y. , Hyodo M. , Hayakawa Y. , Rikihisa Y. . ( 2009; ). The Anaplasma phagocytophilum PleC histidine kinase and PleD diguanylate cyclase two-component system and role of cyclic di-GMP in host cell infection. . J Bacteriol 191:, 693–700. [CrossRef] [PubMed]
    [Google Scholar]
  25. Mattoo S. , Cherry J. D. . ( 2005; ). Molecular pathogenesis, epidemiology, and clinical manifestations of respiratory infections due to Bordetella pertussis and other Bordetella subspecies. . Clin Microbiol Rev 18:, 326–382. [CrossRef] [PubMed]
    [Google Scholar]
  26. McMillan D. J. , Shojaei M. , Chhatwal G. S. , Guzmán C. A. , Walker M. J. . ( 1996; ). Molecular analysis of the bvg-repressed urease of Bordetella bronchiseptica . . Microb Pathog 21:, 379–394. [CrossRef] [PubMed]
    [Google Scholar]
  27. Merkel T. J. , Barros C. , Stibitz S. . ( 1998; ). Characterization of the bvgR locus of Bordetella pertussis . . J Bacteriol 180:, 1682–1690.[PubMed]
    [Google Scholar]
  28. Mikkelsen H. , Ball G. , Giraud C. , Filloux A. . ( 2009; ). Expression of Pseudomonas aeruginosa CupD fimbrial genes is antagonistically controlled by RcsB and the EAL-containing PvrR response regulators. . PLoS ONE 4:, e6018. [CrossRef] [PubMed]
    [Google Scholar]
  29. Mishra M. , Parise G. , Jackson K. D. , Wozniak D. J. , Deora R. . ( 2005; ). The BvgAS signal transduction system regulates biofilm development in Bordetella . . J Bacteriol 187:, 1474–1484. [CrossRef] [PubMed]
    [Google Scholar]
  30. Newell P. D. , Yoshioka S. , Hvorecny K. L. , Monds R. D. , O’Toole G. A. . ( 2011; ). Systematic analysis of diguanylate cyclases that promote biofilm formation by Pseudomonas fluorescens Pf0-1. . J Bacteriol 193:, 4685–4698. [CrossRef] [PubMed]
    [Google Scholar]
  31. Pesavento C. , Becker G. , Sommerfeldt N. , Possling A. , Tschowri N. , Mehlis A. , Hengge R. . ( 2008; ). Inverse regulatory coordination of motility and curli-mediated adhesion in Escherichia coli . . Genes Dev 22:, 2434–2446. [CrossRef] [PubMed]
    [Google Scholar]
  32. Römling U. , Amikam D. . ( 2006; ). Cyclic di-GMP as a second messenger. . Curr Opin Microbiol 9:, 218–228. [CrossRef] [PubMed]
    [Google Scholar]
  33. Sanchez-Torres V. , Hu H. , Wood T. K. . ( 2011; ). GGDEF proteins YeaI, YedQ, and YfiN reduce early biofilm formation and swimming motility in Escherichia coli . . Appl Microbiol Biotechnol 90:, 651–658. [CrossRef] [PubMed]
    [Google Scholar]
  34. Sisti F. , Fernández J. , Rodríguez M. E. , Lagares A. , Guiso N. , Hozbor D. F. . ( 2002; ). In vitro and in vivo characterization of a Bordetella bronchiseptica mutant strain with a deep rough lipopolysaccharide structure. . Infect Immun 70:, 1791–1798. [CrossRef] [PubMed]
    [Google Scholar]
  35. Skinner J. A. , Reissinger A. , Shen H. , Yuk M. H. . ( 2004; ). Bordetella type III secretion and adenylate cyclase toxin synergize to drive dendritic cells into a semimature state. . J Immunol 173:, 1934–1940.[PubMed] [CrossRef]
    [Google Scholar]
  36. Sloan G. P. , Love C. F. , Sukumar N. , Mishra M. , Deora R. . ( 2007; ). The Bordetella Bps polysaccharide is critical for biofilm development in the mouse respiratory tract. . J Bacteriol 189:, 8270–8276. [CrossRef] [PubMed]
    [Google Scholar]
  37. Stainer D. W. , Scholte M. J. . ( 1970; ). A simple chemically defined medium for the production of phase I Bordetella pertussis . . J Gen Microbiol 63:, 211–220.[PubMed] [CrossRef]
    [Google Scholar]
  38. Stockbauer K. E. , Fuchslocher B. , Miller J. F. , Cotter P. A. . ( 2001; ). Identification and characterization of BipA, a Bordetella Bvg-intermediate phase protein. . Mol Microbiol 39:, 65–78. [CrossRef] [PubMed]
    [Google Scholar]
  39. Wan X. , Tuckerman J. R. , Saito J. A. , Freitas T. A. , Newhouse J. S. , Denery J. R. , Galperin M. Y. , Gonzalez G. , Gilles-Gonzalez M. A. , Alam M. . ( 2009; ). Globins synthesize the second messenger bis-(3′–5′)-cyclic diguanosine monophosphate in bacteria. . J Mol Biol 388:, 262–270. [CrossRef] [PubMed]
    [Google Scholar]
  40. Williams C. L. , Cotter P. A. . ( 2007; ). Autoregulation is essential for precise temporal and steady-state regulation by the Bordetella BvgAS phosphorelay. . J Bacteriol 189:, 1974–1982. [CrossRef] [PubMed]
    [Google Scholar]
  41. Wolfe A. J. , Visick K. L. . ( 2008; ). Get the message out: cyclic-di-GMP regulates multiple levels of flagellum-based motility. . J Bacteriol 190:, 463–475. [CrossRef] [PubMed]
    [Google Scholar]
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