Quorum sensing negatively regulates chitinase in Vibrio harveyi.

Quorum sensing, bacterial cell-to-cell communication, regulates the virulence of Vibrio harveyi towards different hosts. Chitinase can be considered as a virulence factor because it helps pathogenic bacteria to attach to the host and to penetrate its tissues (e.g. in case of shrimp). Here, we show that quorum sensing negatively regulates chitinase in V. harveyi. Chitinolytic activity towards natural chitin from crab shells, the synthetic chitin derivative chitin azure, and fluorogenic chitin oligomers was significantly higher in a mutant in which the quorum-sensing system is completely inactivated when compared with a mutant in which the system is maximally active. Furthermore, the addition of signal molecule containing cell-free culture fluids decreased chitinase activity in a Harveyi Autoinducer 1 and Autoinducer 2-deficient double mutant. Finally, chitinase A mRNA levels were fivefold lower in the mutant in which the quorum-sensing system is maximally active when compared with the mutant in which the system is completely inactivated. [Correction added on 25 September 2009, after first online publication: the preceding sentence was corrected from 'Finally, chitinase A mRNA levels were fivefold lower in the mutant in which the quorum-sensing system is completely inactivated when compared with the mutant in which the system is maximally active.'] We argue that this regulation might help the vibrios to switch between host-associated and free-living life styles.

[1]  H. Koley,et al.  Intestinal Adherence of Vibrio cholerae Involves a Coordinated Interaction between Colonization Factor GbpA and Mucin , 2008, Infection and Immunity.

[2]  Bonnie L. Bassler,et al.  The major Vibrio cholerae autoinducer and its role in virulence factor production , 2007, Nature.

[3]  W. Verstraete,et al.  The natural furanone (5Z)-4-bromo-5-(bromomethylene)-3-butyl-2(5H)-furanone disrupts quorum sensing-regulated gene expression in Vibrio harveyi by decreasing the DNA-binding activity of the transcriptional regulator protein luxR. , 2007, Environmental microbiology.

[4]  V. Vuddhakul,et al.  Comparing the efficiency of chitosan with chlorine for reducing Vibrio parahaemolyticus in shrimp , 2007 .

[5]  B. Bassler,et al.  Multiple small RNAs act additively to integrate sensory information and control quorum sensing in Vibrio harveyi. , 2007, Genes & development.

[6]  N. Cianciotto,et al.  Legionella pneumophila type II secretome reveals unique exoproteins and a chitinase that promotes bacterial persistence in the lung , 2006, Proceedings of the National Academy of Sciences.

[7]  W. Verstraete,et al.  Quorum Sensing-Disrupting Brominated Furanones Protect the Gnotobiotic Brine Shrimp Artemia franciscana from Pathogenic Vibrio harveyi, Vibrio campbellii, and Vibrio parahaemolyticus Isolates , 2006, Applied and Environmental Microbiology.

[8]  Brooke A. Jude,et al.  A colonization factor links Vibrio cholerae environmental survival and human infection , 2005, Nature.

[9]  F. Ascencio,et al.  A review of extracellular virulence product of Vibrio species important in diseases of cultivated shrimp , 2004 .

[10]  Bonnie L. Bassler,et al.  Three Parallel Quorum-Sensing Systems Regulate Gene Expression in Vibrio harveyi , 2004, Journal of bacteriology.

[11]  B. Bassler,et al.  Quorum Sensing Regulates Type III Secretion in Vibrio harveyi and Vibrio parahaemolyticus , 2004, Journal of bacteriology.

[12]  R. Camarillo,et al.  Colloidal chitin stained with Remazol Brilliant Blue R®, a useful substrate to select chitinolytic microorganisms and to evaluate chitinases , 2004 .

[13]  Bonnie L Bassler,et al.  Chemical communication among bacteria , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[14]  R. Weiner,et al.  Detection and characterization of chitinases and other chitin-modifying enzymes , 2003, Journal of Industrial Microbiology and Biotechnology.

[15]  Jun Zhu,et al.  Quorum sensing-dependent biofilms enhance colonization in Vibrio cholerae. , 2003, Developmental cell.

[16]  Ned S Wingreen,et al.  Vibrio harveyi quorum sensing: a coincidence detector for two autoinducers controls gene expression , 2003, The EMBO journal.

[17]  B. Bassler,et al.  Structural identification of a bacterial quorum-sensing signal containing boron , 2002, Nature.

[18]  L. Fothergill-Gilmore,et al.  Chitinases from Vibrio: activity screening and purification of chiA from Vibrio carchariae , 2000, Journal of applied microbiology.

[19]  B. Bassler,et al.  Regulation of quorum sensing in Vibrio harveyi by LuxO and Sigma‐54 , 2000, Molecular microbiology.

[20]  S. Rice,et al.  Inhibition of Luminescence and Virulence in the Black Tiger Prawn (Penaeus monodon) Pathogen Vibrio harveyi by Intercellular Signal Antagonists , 2000, Applied and Environmental Microbiology.

[21]  S. Roseman,et al.  Physiological aspects of chitin catabolism in marine bacteria. , 1999, Biochimica et biophysica acta.

[22]  B. Bassler,et al.  A genetic analysis of the function of LuxO, a two‐component response regulator involved in quorum sensing in Vibrio harveyi , 1999, Molecular microbiology.

[23]  M. Winson,et al.  Chitinolytic Activity in Chromobacterium violaceum: Substrate Analysis and Regulation by Quorum Sensing , 1998, Journal of bacteriology.

[24]  E. Greenberg,et al.  Cross-species induction of luminescence in the quorum-sensing bacterium Vibrio harveyi , 1997, Journal of bacteriology.

[25]  D. Kirchman,et al.  Chitin Degradation Proteins Produced by the Marine Bacterium Vibrio harveyi Growing on Different Forms of Chitin , 1997, Applied and environmental microbiology.

[26]  Rita R. Colwell.  Global Climate and Infectious Disease: The Cholera Paradigm* , 1996, Science.

[27]  B. Bassler,et al.  Intercellular signalling in Vibrio harveyi: sequence and function of genes regulating expression of luminescence , 1993, Molecular microbiology.

[28]  E. Meighen,et al.  Purification and structural identification of an autoinducer for the luminescence system of Vibrio harveyi. , 1989, The Journal of biological chemistry.

[29]  W. Verstraete,et al.  Quorum sensing and quorum quenching in Vibrio harveyi: lessons learned from in vivo work , 2008, The ISME Journal.