Extracellular nucleases and extracellular DNA play important roles in Vibrio cholerae biofilm formation

Abstract

Biofilms are a preferred mode of survival for many microorganisms including Vibrio cholerae, the causative agent of the severe secretory diarrhoeal disease cholera. The ability of the facultative human pathogen V. cholerae to form biofilms is a key factor for persistence in aquatic ecosystems and biofilms act as a source for new outbreaks. Thus, a better understanding of biofilm formation and transmission of V. cholerae is an important target to control the disease. So far the Vibrio exopolysaccharide was the only known constituent of the biofilm matrix. In this study we identify and characterize extracellular DNA as a component of the Vibrio biofilm matrix. Furthermore, we show that extracellular DNA is modulated and controlled by the two extracellular nucleases Dns and Xds. Our results indicate that extracellular DNA and the extracellular nucleases are involved in diverse processes including the development of a typical biofilm architecture, nutrient acquisition, detachment from biofilms and the colonization fitness of biofilm clumps after ingestion by the host. This study provides new insights into biofilm development and transmission of biofilm-derived V. cholerae.

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     Not in our library10.1128/jb.112.2.932-939.1972

102. 102.

     Steinberger RE, Holden PA. Extracellular DNA in single- and multiple-species unsaturated biofilms. Appl Environ Microbiol. 2005;71:5404-5410.

     Not in our library10.1128/aem.71.9.5404-5410.2005

103. 103.

     Sternberg C, Tolker-Nielsen T. Growing and analyzing biofilms in flow cells. Curr Protoc Microbiol. 2006.

     Not in our library10.1002/9780471729259.mc01b02s00

104. 104.

     Sternberg C, Christensen BB, Johansen T, Toftgaard Nielsen A, Andersen JB, Givskov M, Molin S. Distribution of bacterial growth activity in flow-chamber biofilms. Appl Environ Microbiol. 1999;65:4108-4117.

     Not in our library10.1128/aem.65.9.4108-4117.1999

105. 105.

     Tamayo R, Schild S, Pratt JT, Camilli A. Role of cyclic Di-GMP during el tor biotype Vibrio cholerae infection: characterization of the in vivo-induced cyclic Di-GMP phosphodiesterase CdpA. Infect Immun. 2008;76:1617-1627.

     Not in our library10.1128/iai.01337-07

106. 106.

     Tamayo R, Patimalla B, Camilli A. Growth in a biofilm induces a hyperinfectious phenotype in Vibrio cholerae. Infect Immun. 2010;78:3560-3569.

     Not in our library10.1128/iai.00048-10

107. 107.

     Tamplin ML, Gauzens AL, Huq A, Sack DA, Colwell RR. Attachment of Vibrio cholerae serogroup O1 to zooplankton and phytoplankton of Bangladesh waters. Appl Environ Microbiol. 1990;56:1977-1980.

     Not in our library10.1128/aem.56.6.1977-1980.1990

108. 108.

     Thomas VC, Thurlow LR, Boyle D, Hancock LE. Regulation of autolysis-dependent extracellular DNA release by Enterococcus faecalis extracellular proteases influences biofilm development. J Bacteriol. 2008;190:5690-5698.

     Not in our library10.1128/jb.00314-08

109. 109.

     Tipper DJ. Mechanism of autolysis of isolated cell walls of Staphylococcus aureus. J Bacteriol. 1969;97:837-847.

     Not in our library10.1128/jb.97.2.837-847.1969

110. 110.

     Tischler AD, Camilli A. Cyclic diguanylate (c-di-GMP) regulates Vibrio cholerae biofilm formation. Mol Microbiol. 2004;53:857-869.

     Not in our library10.1111/j.1365-2958.2004.04155.x

111. 111.

     Tischler AD, Camilli A. Cyclic diguanylate regulates Vibrio cholerae virulence gene expression. Infect Immun. 2005;73:5873-5882.

     Not in our library10.1128/iai.73.9.5873-5882.2005

112. 112.

     Trevors JT. DNA in soil: adsorption, genetic transformation, molecular evolution and genetic microchip. Antonie Van Leeuwenhoek. 1996;70:1-10.

     Not in our library10.1007/bf00393564

113. 113.

     Udden SM, Zahid MS, Biswas K, Ahmad QS, Cravioto A, Nair GB, et al. Acquisition of classical CTX prophage from Vibrio cholerae O141 by El Tor strains aided by lytic phages and chitin-induced competence. Proc Natl Acad Sci USA. 2008;105:11951-11956.

     Not in our library10.1073/pnas.0805560105

114. 114.

     Vlassov VV, Laktionov PP, Rykova EY. Extracellular nucleic acids. Bioessays. 2007;29:654-667.

     Not in our library10.1002/bies.20604

115. 115.

     Vollmer W, Joris B, Charlier P, Foster S. Bacterial peptidoglycan (murein) hydrolases. FEMS Microbiol Rev. 2008;32:259-286.

     Not in our library10.1111/j.1574-6976.2007.00099.x

116. 116.

     Waters CM, Lu W, Rabinowitz JD, Bassler BL. Quorum sensing controls biofilm formation in Vibrio cholerae through modulation of cyclic di-GMP levels and repression of vpsT. J Bacteriol. 2008;190:2527-2536.

     Not in our library10.1128/jb.01756-07

117. 117.

     Watnick P, Kolter R. Steps in the develompent of a Vibrio cholerae El Tor biofilm. Mol Microbiol. 1999;34:586-595.

     Not in our library10.1046/j.1365-2958.1999.01624.x

118. 118.

     Watnick PI, Fullner KJ, Kolter R. A Role for the Mannose-Sensitive Hemagglutinin in Biofilm Formation by Vibrio cholerae El Tor. J Bacteriol. 1999;181:3606-3609.

     Not in our library10.1128/jb.181.11.3606-3609.1999

119. 119.

     Watnick PI, Lauriano CM, Klose KE, Croal L, Kolter R. The absence of a flagellum leads to altered colony morphology, biofilm development and virulence in Vibrio cholerae O139. Mol Microbiol. 2001;39:223-235.

     Not in our library10.1046/j.1365-2958.2001.02195.x

120. 120.

     Whitchurch CB, Tolker-Nielsen T, Ragas PC, Mattick JS. Extracellular DNA required for bacterial biofilm formation. Science. 2002;295:1487.

     Not in our library10.1126/science.295.5559.1487

121. 121.

     Cholera, 2008. Wkly Epidemiol Rec. 2009;31:309-324.

     Not in our library

122. 122.

     Yang M, Frey EM, Liu Z, Bishar R, Zhu J. The virulence transcriptional activator AphA enhances biofilm formation of Vibrio cholerae by activating the expression of the biofilm regulator VpsT. Infect Immun. 2009;78:697-703.

     Not in our library10.1128/iai.00429-09

123. 123.

     Yang X, Beyenal H, Harkin G, Lewandowski Z. Quantifying biofilm structure using image analysis. J Microbiol Methods. 2000;39:109-119.

     Not in our library10.1016/s0167-7012(99)00097-4

124. 124.

     Yaron S, Kolling GL, Simon L, Matthews KR. Vesicle-mediated transfer of virulence genes from Escherichia coli O157:H7 to other enteric bacteria. Appl Environ Microbiol. 2000;66:4414-4420.

     Not in our library10.1128/aem.66.10.4414-4420.2000

125. 125.

     Yildiz FH, Schoolnik GK. Vibrio cholerae O1 El Tor: Identification of a gene cluster required for the rugose colony type, exopolysaccharide production, chlorine resistance, and biofilm formation. Proc Natl Acad Sci USA. 1999;96:4028-4033.

     Not in our library10.1073/pnas.96.7.4028

126. 126.

     Yildiz FH, Visick KL. Vibrio biofilms: so much the same yet so different. Trends Microbiol. 2009;17:109-118.

     Not in our library10.1016/j.tim.2008.12.004

127. 127.

     Yildiz FH, Dolganov NA, Schoolnik GK. VpsR, a Member of the Response Regulators of the Two-Component Regulatory Systems, Is Required for Expression of vps Biosynthesis Genes and EPS(ETr)-Associated Phenotypes in Vibrio cholerae O1 El Tor. J Bacteriol. 2001;183:1716-1726.

     Not in our library10.1128/jb.183.5.1716-1726.2001

128. 128.

     Yildiz FH, Liu XS, Heydorn A, Schoolnik GK. Molecular analysis of rugosity in a Vibrio cholerae O1 El Tor phase variant. Mol Microbiol. 2004;53:497-515.

     Not in our library10.1111/j.1365-2958.2004.04154.x

129. 129.

     Zhu J, Mekalanos JJ. Quorum sensing-dependent biofilms enhance colonization in Vibrio cholerae. Dev Cell. 2003;5:647-656.

     Not in our library10.1016/s1534-5807(03)00295-8

Cited by papers we hold 17

• Strategy to combat biofilms: a focus on biofilm dispersal enzymes · 2023
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• Mimicking biofilm formation and development: Recent progress in in vitro and in vivo biofilm models · 2021
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• Biofilms by bacterial human pathogens: Clinical relevance - development, composition and regulation - therapeutical strategies · 2021
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• Deoxyribonucleases and Their Applications in Biomedicine · 2020
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• Targeting Biofilms Therapy: Current Research Strategies and Development Hurdles · 2020
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• Extracellular DNA in natural environments: features, relevance and applications · 2018
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• Approaches to Dispersing Medical Biofilms · 2017
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• Microbial Extracellular Polymeric Substances (EPSs) in Ocean Systems · 2017
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• Mechanisms and Regulation of Extracellular DNA Release and Its Biological Roles in Microbial Communities · 2017
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• A novel mechanism for the biogenesis of outer membrane vesicles in Gram-negative bacteria · 2016
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• Vibrio cholerae Biofilms and Cholera Pathogenesis · 2016
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• Antibacterial activity of silver and zinc nanoparticles against Vibrio cholerae and enterotoxic Escherichia coli · 2015
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• C-di-GMP Regulates Motile to Sessile Transition by Modulating MshA Pili Biogenesis and Near-Surface Motility Behavior in Vibrio cholerae · 2015
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• Environmental reservoirs and mechanisms of persistence of Vibrio cholerae · 2013
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• Vibrio cholerae Evades Neutrophil Extracellular Traps by the Activity of Two Extracellular Nucleases · 2013
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• Identification of a General O-linked Protein Glycosylation System in Acinetobacter baumannii and Its Role in Virulence and Biofilm Formation · 2012
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• The Regulatory Network of Natural Competence and Transformation of Vibrio cholerae · 2012
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