Previous Article | Next Article 
Journal of Bacteriology, February 2003, p. 1384-1390, Vol. 185, No. 4
0021-9193/03/$08.00+0 DOI: 10.1128/JB.185.4.1384-1390.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.
Identification and Characterization of a Vibrio cholerae Gene, mbaA, Involved in Maintenance of Biofilm Architecture
Natalia Bomchil, Paula Watnick,
and Roberto Kolter*
Department of Microbiology and Molecular Genetics, Harvard Medical School, Boston, Massachusetts 02115
Received 29 July 2002/
Accepted 11 October 2002
The formation of biofilms is thought to play a key role in the environmental survival of the marine bacterium Vibrio cholerae. Although the factors involved in V. cholerae attachment to abiotic surfaces have been extensively studied, relatively little is known about the mechanisms involved in the subsequent maturation of the biofilms. Here we report the identification of a novel gene, which we have named mbaA (for maintenance of biofilm architecture), that plays a role in the formation and maintenance of the highly organized three-dimensional architecture of V. cholerae El Tor biofilms. We demonstrate that although the absence of mbaA does not significantly affect the initial attachment of cells onto the surface, it leads to the formation of biofilms that lack the typical structure, including the pillars of cells separated by fluid-filled channels that are evident in mature wild-type biofilms. Microscopic analysis indicates that the absence of mbaA leads to an increase in the amount of extracellular matrix material in the biofilms. The predicted mbaA product is a member of a family of regulatory proteins, containing GGDEF and EAL domains, suggesting that MbaA regulates the synthesis of some component of the biofilm matrix.
* Corresponding author. Mailing address: Department of Microbiology and Molecular Genetics, Harvard Medical School, 200 Longwood Ave., Boston, MA 02115. Phone: (617) 432-1776. Fax: (617) 738-7664. E-mail:
rkolter{at}hms.harvard.edu.
Present address: Division of Geographic Medicine and Infectious Disease, New England Medical Center, Boston, MA 02111.
Journal of Bacteriology, February 2003, p. 1384-1390, Vol. 185, No. 4
0021-9193/03/$08.00+0 DOI: 10.1128/JB.185.4.1384-1390.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.
This article has been cited by other articles:
-
Almagro-Moreno, S., Boyd, E. F.
(2009). Sialic Acid Catabolism Confers a Competitive Advantage to Pathogenic Vibrio cholerae in the Mouse Intestine. Infect. Immun.
77: 3807-3816
[Abstract]
[Full Text]
-
Karatan, E., Watnick, P.
(2009). Signals, Regulatory Networks, and Materials That Build and Break Bacterial Biofilms. Microbiol. Mol. Biol. Rev.
73: 310-347
[Abstract]
[Full Text]
-
Hammer, B. K., Bassler, B. L.
(2009). Distinct Sensory Pathways in Vibrio cholerae El Tor and Classical Biotypes Modulate Cyclic Dimeric GMP Levels To Control Biofilm Formation. J. Bacteriol.
191: 169-177
[Abstract]
[Full Text]
-
Beyhan, S., Odell, L. S., Yildiz, F. H.
(2008). Identification and Characterization of Cyclic Diguanylate Signaling Systems Controlling Rugosity in Vibrio cholerae. J. Bacteriol.
190: 7392-7405
[Abstract]
[Full Text]
-
Shah, S., Das, B., Bhadra, R. K.
(2008). Functional Analysis of the Essential GTP-Binding-Protein-Coding Gene cgtA of Vibrio cholerae. J. Bacteriol.
190: 4764-4771
[Abstract]
[Full Text]
-
Ferreira, R. B. R., Antunes, L. C. M., Greenberg, E. P., McCarter, L. L.
(2008). Vibrio parahaemolyticus ScrC Modulates Cyclic Dimeric GMP Regulation of Gene Expression Relevant to Growth on Surfaces. J. Bacteriol.
190: 851-860
[Abstract]
[Full Text]
-
Kim, Y.-K., McCarter, L. L.
(2007). ScrG, a GGDEF-EAL Protein, Participates in Regulating Swarming and Sticking in Vibrio parahaemolyticus. J. Bacteriol.
189: 4094-4107
[Abstract]
[Full Text]
-
Malone, J. G., Williams, R., Christen, M., Jenal, U., Spiers, A. J., Rainey, P. B.
(2007). The structure-function relationship of WspR, a Pseudomonas fluorescens response regulator with a GGDEF output domain. Microbiology
153: 980-994
[Abstract]
[Full Text]
-
Karaolis, D. K. R., Means, T. K., Yang, D., Takahashi, M., Yoshimura, T., Muraille, E., Philpott, D., Schroeder, J. T., Hyodo, M., Hayakawa, Y., Talbot, B. G., Brouillette, E., Malouin, F.
(2007). Bacterial c-di-GMP Is an Immunostimulatory Molecule. J. Immunol.
178: 2171-2181
[Abstract]
[Full Text]
-
Parise, G., Mishra, M., Itoh, Y., Romeo, T., Deora, R.
(2007). Role of a Putative Polysaccharide Locus in Bordetella Biofilm Development. J. Bacteriol.
189: 750-760
[Abstract]
[Full Text]
-
Lim, B., Beyhan, S., Yildiz, F. H.
(2007). Regulation of Vibrio Polysaccharide Synthesis and Virulence Factor Production by CdgC, a GGDEF-EAL Domain Protein, in Vibrio cholerae. J. Bacteriol.
189: 717-729
[Abstract]
[Full Text]
-
Liu, Z., Stirling, F. R., Zhu, J.
(2007). Temporal Quorum-Sensing Induction Regulates Vibrio cholerae Biofilm Architecture. Infect. Immun.
75: 122-126
[Abstract]
[Full Text]
-
Ryan, R. P., Fouhy, Y., Lucey, J. F., Dow, J. M.
(2006). Cyclic Di-GMP Signaling in Bacteria: Recent Advances and New Puzzles. J. Bacteriol.
188: 8327-8334
[Full Text]
-
Hsiao, A., Liu, Z., Joelsson, A., Zhu, J.
(2006). Vibrio cholerae virulence regulator-coordinated evasion of host immunity. Proc. Natl. Acad. Sci. USA
103: 14542-14547
[Abstract]
[Full Text]
-
Davey, M. E., Duncan, M. J.
(2006). Enhanced Biofilm Formation and Loss of Capsule Synthesis: Deletion of a Putative Glycosyltransferase in Porphyromonas gingivalis.. J. Bacteriol.
188: 5510-5523
[Abstract]
[Full Text]
-
Paddick, J. S., Brailsford, S. R., Rao, S., Soares, R. F., Kidd, E. A. M., Beighton, D., Homer, K. A.
(2006). Effect of Biofilm Growth on Expression of Surface Proteins of Actinomyces naeslundii Genospecies 2.. Appl. Environ. Microbiol.
72: 3774-3779
[Abstract]
[Full Text]
-
Beyhan, S., Tischler, A. D., Camilli, A., Yildiz, F. H.
(2006). Transcriptome and Phenotypic Responses of Vibrio cholerae to Increased Cyclic di-GMP Level.. J. Bacteriol.
188: 3600-3613
[Abstract]
[Full Text]
-
Da Re, S., Ghigo, J.-M.
(2006). A CsgD-Independent Pathway for Cellulose Production and Biofilm Formation in Escherichia coli.. J. Bacteriol.
188: 3073-3087
[Abstract]
[Full Text]
-
Kulasakara, H., Lee, V., Brencic, A., Liberati, N., Urbach, J., Miyata, S., Lee, D. G., Neely, A. N., Hyodo, M., Hayakawa, Y., Ausubel, F. M., Lory, S.
(2006). Analysis of Pseudomonas aeruginosa diguanylate cyclases and phosphodiesterases reveals a role for bis-(3'-5')-cyclic-GMP in virulence. Proc. Natl. Acad. Sci. USA
103: 2839-2844
[Abstract]
[Full Text]
-
Fong, J. C. N., Karplus, K., Schoolnik, G. K., Yildiz, F. H.
(2006). Identification and Characterization of RbmA, a Novel Protein Required for the Development of Rugose Colony Morphology and Biofilm Structure in Vibrio cholerae. J. Bacteriol.
188: 1049-1059
[Abstract]
[Full Text]
-
Karatan, E., Duncan, T. R., Watnick, P. I.
(2005). NspS, a Predicted Polyamine Sensor, Mediates Activation of Vibrio cholerae Biofilm Formation by Norspermidine. J. Bacteriol.
187: 7434-7443
[Abstract]
[Full Text]
-
Hickman, J. W., Tifrea, D. F., Harwood, C. S.
(2005). A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels. Proc. Natl. Acad. Sci. USA
102: 14422-14427
[Abstract]
[Full Text]
-
Christen, M., Christen, B., Folcher, M., Schauerte, A., Jenal, U.
(2005). Identification and Characterization of a Cyclic di-GMP-specific Phosphodiesterase and Its Allosteric Control by GTP. J. Biol. Chem.
280: 30829-30837
[Abstract]
[Full Text]
-
Brouillette, E., Hyodo, M., Hayakawa, Y., Karaolis, D. K. R., Malouin, F.
(2005). 3',5'-Cyclic Diguanylic Acid Reduces the Virulence of Biofilm-Forming Staphylococcus aureus Strains in a Mouse Model of Mastitis Infection. Antimicrob. Agents Chemother.
49: 3109-3113
[Abstract]
[Full Text]
-
Kirn, T. J., Taylor, R. K.
(2005). TcpF Is a Soluble Colonization Factor and Protective Antigen Secreted by El Tor and Classical O1 and O139 Vibrio cholerae Serogroups. Infect. Immun.
73: 4461-4470
[Abstract]
[Full Text]
-
Schmidt, A. J., Ryjenkov, D. A., Gomelsky, M.
(2005). The Ubiquitous Protein Domain EAL Is a Cyclic Diguanylate-Specific Phosphodiesterase: Enzymatically Active and Inactive EAL Domains. J. Bacteriol.
187: 4774-4781
[Abstract]
[Full Text]
-
Karaolis, D. K. R., Rashid, M. H., Chythanya, R., Luo, W., Hyodo, M., Hayakawa, Y.
(2005). c-di-GMP (3'-5'-Cyclic Diguanylic Acid) Inhibits Staphylococcus aureus Cell-Cell Interactions and Biofilm Formation. Antimicrob. Agents Chemother.
49: 1029-1038
[Abstract]
[Full Text]
-
Ryjenkov, D. A., Tarutina, M., Moskvin, O. V., Gomelsky, M.
(2005). Cyclic Diguanylate Is a Ubiquitous Signaling Molecule in Bacteria: Insights into Biochemistry of the GGDEF Protein Domain. J. Bacteriol.
187: 1792-1798
[Abstract]
[Full Text]
-
Choy, W.-K., Zhou, L., Syn, C. K.-C., Zhang, L.-H., Swarup, S.
(2004). MorA Defines a New Class of Regulators Affecting Flagellar Development and Biofilm Formation in Diverse Pseudomonas Species. J. Bacteriol.
186: 7221-7228
[Abstract]
[Full Text]
-
D'Argenio, D. A., Miller, S. I.
(2004). Cyclic di-GMP as a bacterial second messenger. Microbiology
150: 2497-2502
[Abstract]
[Full Text]
-
Paul, R., Weiser, S., Amiot, N. C., Chan, C., Schirmer, T., Giese, B., Jenal, U.
(2004). Cell cycle-dependent dynamic localization of a bacterial response regulator with a novel di-guanylate cyclase output domain. Genes Dev.
18: 715-727
[Abstract]
[Full Text]
-
Guvener, Z. T., McCarter, L. L.
(2003). Multiple Regulators Control Capsular Polysaccharide Production in Vibrio parahaemolyticus. J. Bacteriol.
185: 5431-5441
[Abstract]
[Full Text]
-
Battin, T. J., Kaplan, L. A., Newbold, J. D., Cheng, X., Hansen, C.
(2003). Effects of Current Velocity on the Nascent Architecture of Stream Microbial Biofilms. Appl. Environ. Microbiol.
69: 5443-5452
[Abstract]
[Full Text]