The Bvg Virulence Control System Regulates Biofilm Formation in Bordetella bronchiseptica

ABSTRACT Bordetella species utilize the BvgAS (Bordetella virulence gene) two-component signal transduction system to sense the environment and regulate gene expression among at least three phases: a virulent Bvg+ phase, a nonvirulent Bvg− phase, and an intermediate Bvgi phase. Genes expressed in the Bvg+ phase encode known virulence factors, including adhesins such as filamentous hemagglutinin (FHA) and fimbriae, as well as toxins such as the bifunctional adenylate cyclase/hemolysin (ACY). Previous studies showed that in the Bvgi phase, FHA and fimbriae continue to be expressed, but ACY expression is significantly downregulated. In this report, we determine that Bordetella bronchiseptica can form biofilms in vitro and that the generation of biofilm is maximal in the Bvgi phase. We show that FHA is required for maximal biofilm formation and that fimbriae may also contribute to this phenotype. However, expression of ACY inhibits biofilm formation, most likely via interactions with FHA. Therefore, the coordinated regulation of adhesins and ACY expression leads to maximal biofilm formation in the Bvgi phase in B. bronchiseptica.

[1]  E. Hewlett,et al.  Mechanism of association of adenylate cyclase toxin with the surface of Bordetella pertussis: a role for toxin–filamentous haemagglutinin interaction , 2002, Molecular microbiology.

[2]  Jeff F. Miller,et al.  Identification and characterization of BipA, a Bordetella Bvg‐intermediate phase protein , 2001, Molecular microbiology.

[3]  Jeff F. Miller,et al.  Ectopic expression of the flagellar regulon alters development of the bordetella-host interaction , 1995, Cell.

[4]  G. Rettinger,et al.  Nasal mucosal temperature during respiration. , 2002, Clinical otolaryngology and allied sciences.

[5]  F. Mooi,et al.  Construction and analysis of Bordetella pertussis mutants defective in the production of fimbriae. , 1992, Microbial pathogenesis.

[6]  C. Locht,et al.  The filamentous haemagglutinin, a multifaceted adhesin produced by virulent Bordetella spp. , 1993, Molecular microbiology.

[7]  M. Parsek,et al.  Bacterial biofilms: an emerging link to disease pathogenesis. , 2003, Annual review of microbiology.

[8]  W. Kay,et al.  Thin aggregative fimbriae enhance Salmonella enteritidis biofilm formation. , 1998, FEMS microbiology letters.

[9]  Jeff F. Miller,et al.  Role of Bordetella bronchisepticaFimbriae in Tracheal Colonization and Development of a Humoral Immune Response , 2000, Infection and Immunity.

[10]  J. Miller,et al.  Mechanisms of Bordetella pathogenesis. , 2001, Frontiers in bioscience : a journal and virtual library.

[11]  K. Lewis,et al.  Riddle of Biofilm Resistance , 2001, Antimicrobial Agents and Chemotherapy.

[12]  P. Watnick,et al.  Genetic approaches to study of biofilms. , 1999, Methods in enzymology.

[13]  B. Lacey.  Antigenic modulation of Bordetella pertussis , 1960, Journal of Hygiene.

[14]  D. Relman,et al.  Filamentous Hemagglutinin of Bordetella bronchiseptica Is Required for Efficient Establishment of Tracheal Colonization , 1998, Infection and Immunity.

[15]  S. Falkow,et al.  The bvgAS locus negatively controls motility and synthesis of flagella in Bordetella bronchiseptica , 1992, Journal of bacteriology.

[16]  D A Turner,et al.  Use of intrinsic optical signals to monitor physiological changes in brain tissue slices. , 1999, Methods.

[17]  Jeff F. Miller,et al.  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 , 1997, Molecular microbiology.

[18]  S. Kjelleberg,et al.  Is there a role for quorum sensing signals in bacterial biofilms? , 2002, Current opinion in microbiology.

[19]  J. Miller,et al.  BvgAS-mediated signal transduction: analysis of phase-locked regulatory mutants of Bordetella bronchiseptica in a rabbit model , 1994, Infection and immunity.

[20]  P. Watnick,et al.  Biofilm, City of Microbes , 2000 .

[21]  Allison M. Jones,et al.  Phosphorelay control of virulence gene expression in Bordetella. , 2003, Trends in microbiology.

[22]  W. M. R. Akker.  The Filamentous Hemagglutinin ofBordetella parapertussisIs the Major Adhesin in the Phase-Dependent Interaction with NCI-H292 Human Lung Epithelial Cells , 1998 .

[23]  A. Jesaitis,et al.  Compromised Host Defense on Pseudomonas aeruginosa Biofilms: Characterization of Neutrophil and Biofilm Interactions 1 , 2003, The Journal of Immunology.

[24]  J. Costerton,et al.  Bacterial biofilms: a common cause of persistent infections. , 1999, Science.

[25]  R. Kolter,et al.  Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development , 1998, Molecular microbiology.

[26]  S. Molin,et al.  Biofilm formation by Pseudomonas aeruginosa wild type, flagella and type IV pili mutants , 2003, Molecular microbiology.

[27]  W. V. D. van den Akker.  The filamentous hemagglutinin of Bordetella parapertussis is the major adhesin in the phase-dependent interaction with NCI-H292 human lung epithelial cells. , 1998, Biochemical and biophysical research communications.

[28]  D. Allison,et al.  Extracellular products as mediators of the formation and detachment of Pseudomonas fluorescens biofilms. , 1998, FEMS microbiology letters.

[29]  D. Relman,et al.  Bordetella Species Are Distinguished by Patterns of Substantial Gene Loss and Host Adaptation , 2004, Journal of bacteriology.

[30]  D W Stainer,et al.  A simple chemically defined medium for the production of phase I Bordetella pertussis. , 1970, Journal of general microbiology.

[31]  D. Ladant,et al.  Bordetella pertussis adenylate cyclase: a toxin with multiple talents. , 1993, Zentralblatt fur Bakteriologie : international journal of medical microbiology.

[32]  Søren Molin,et al.  Involvement of bacterial migration in the development of complex multicellular structures in Pseudomonas aeruginosa biofilms , 2003, Molecular microbiology.

[33]  R. Kolter,et al.  Biofilm formation as microbial development. , 2000, Annual review of microbiology.

[34]  B. Barrell,et al.  Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica , 2003, Nature Genetics.

[35]  Jeff F. Miller,et al.  Probing the Function of Bordetella bronchiseptica Adenylate Cyclase Toxin by Manipulating Host Immunity , 1999, Infection and Immunity.

[36]  S. Kjelleberg,et al.  Cell Death in Pseudomonas aeruginosa Biofilm Development , 2003, Journal of bacteriology.

[37]  S. Kjelleberg,et al.  Bacterial biofilms: prokaryotic adventures in multicellularity. , 2003, Current opinion in microbiology.

[38]  E. Tuomanen,et al.  Filamentous hemagglutinin and pertussis toxin promote adherence of Bordetella pertussis to cilia. , 1985, Developments in biological standardization.