Skip to content
naulon

No retraction, correction or concern found when last checked on Nov 4, 2026.

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

Andrea Seper, Vera H. I. Fengler, Sandro Roier and 6 more

Molecular Microbiology · 2011

doi:10.1111/j.1365-2958.2011.07867.x

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.

Shown for reading. Its publisher allows quoting it, not republishing it.

References 129

  1. 1.

    Alam M, Sultana M, Nair GB, Siddique AK, Hasan NA, Sack RB, et al. Viable but nonculturable Vibrio cholerae O1 in biofilms in the aquatic environment and their role in cholera transmission. Proc Natl Acad Sci USA. 2007;104:17801-17806.

    Not in our library10.1073/pnas.0705599104

  2. 2.

    Altermark B, Niiranen L, Willassen NP, Smalas AO, Moe E. Comparative studies of endonuclease I from cold-adapted Vibrio salmonicida and mesophilic Vibrio cholerae. FEBS J. 2007;274:252-263.

    Not in our library10.1111/j.1742-4658.2006.05580.x

  3. 3.

    Berne C, Kysela DT, Brun YV. A bacterial extracellular DNA inhibits settling of motile progeny cells within a biofilm. Mol Microbiol. 2010;77:815-829.

    Not in our library10.1111/j.1365-2958.2010.07267.x

  4. 4.

    Beyhan S, Bilecen K, Salama SR, Casper-Lindley C, Yildiz FH. Regulation of rugosity and biofilm formation in Vibrio cholerae: comparison of VpsT and VpsR regulons and epistasis analysis of vpsT, vpsR, and hapR. J Bacteriol. 2007;189:388-402.

    Not in our library10.1128/jb.00981-06

  5. 5.

    Bik EM, Bunschoten AE, Gouw RD, Mooi FR. Genesis of the novel epidemic Vibrio cholerae O139 strain: evidence for horizontal transfer of genes involved in polysaccharide synthesis. EMBO J. 1995;14:209-216.

    Not in our library10.1002/j.1460-2075.1995.tb06993.x

  6. 6.
  7. 7.

    Blokesch M, Schoolnik GK. The extracellular nuclease Dns and its role in natural transformation of Vibrio cholerae. J Bacteriol. 2008;190:7232-7240.

    Not in our library10.1128/jb.00959-08

  8. 8.

    Bomchil N, Watnick P, Kolter R. Identification and characterization of a Vibrio cholerae gene, mbaA, involved in maintenance of biofilm architecture. J Bacteriol. 2003;185:1384-1390.

    Not in our library10.1128/jb.185.4.1384-1390.2003

  9. 9.

    Butler SM, Camilli A. Both chemotaxis and net motility greatly influence the infectivity of Vibrio cholerae. Proc Natl Acad Sci USA. 2004;101:5018-5023.

    Not in our library10.1073/pnas.0308052101

  10. 10.

    Butler SM, Camilli A. Going against the grain: chemotaxis and infection in Vibrio cholerae. Nat Rev Microbiol. 2005;3:611-620.

    Not in our library10.1038/nrmicro1207

  11. 11.

    Casper-Lindley C, Yildiz FH. VpsT is a transcriptional regulator required for expression of vps biosynthesis genes and the development of rugose colonial morphology in Vibrio cholerae O1 El Tor. J Bacteriol. 2004;186:1574-1578.

    Not in our library10.1128/jb.186.5.1574-1578.2004

  12. 12.

    Chatterjee SN, Das J. Electron microscopic observations on the excretion of cell-wall material by Vibrio cholerae. J Gen Microbiol. 1967;49:1-11.

    Not in our library10.1099/00221287-49-1-1

  13. 13.

    Chiavelli DA, Marsh JW, Taylor RK. The mannose-sensitive hemagglutinin of Vibrio cholerae promotes adherence to zooplankton. Appl Environ Microbiol. 2001;67:3220-3225.

    Not in our library10.1128/aem.67.7.3220-3225.2001

  14. 14.

    Colwell RR. Global climate and infectious disease: the cholera paradigm. Science. 1996;274:2025-2031.

    Not in our library10.1126/science.274.5295.2025

  15. 15.

    Colwell RR, Huq A, Islam MS, Aziz KM, Yunus M, Khan NH, et al. Reduction of cholera in Bangladeshi villages by simple filtration. Proc Natl Acad Sci USA. 2003;100:1051-1055.

    Not in our library10.1073/pnas.0237386100

  16. 16.

    Conover MS, Mishra M, Deora R. Extracellular DNA is essential for maintaining Bordetella biofilm integrity on abiotic surfaces and in the upper respiratory tract of mice. PLoS ONE. 2011;6:e16861.

    Not in our library10.1371/journal.pone.0016861

  17. 17.

    Dell'Anno A, Danovaro R. Extracellular DNA plays a key role in deep-sea ecosystem functioning. Science. 2005;309:2179.

    Not in our library10.1126/science.1117475

  18. 18.

    Dlakic M. Functionally unrelated signalling proteins contain a fold similar to Mg2+-dependent endonucleases. Trends Biochem Sci. 2000;25:272-273.

    Not in our library10.1016/s0968-0004(00)01582-6

  19. 19.

    Donnenberg MS, Kaper JB. Construction of an eae deletion mutant of enteropathogenic Escherichia coli by using a positive-selection suicide vector. Infect Immun. 1991;59:4310-4317.

    Not in our library10.1128/iai.59.12.4310-4317.1991

  20. 20.

    Dorward DW, Garon CF, Judd RC. Export and intercellular transfer of DNA via membrane blebs of Neisseria gonorrhoeae. J Bacteriol. 1989;171:2499-2505.

    Not in our library10.1128/jb.171.5.2499-2505.1989

  21. 21.

    Faruque SM, Albert MJ, Mekalanos JJ. Epidemiology, genetics, and ecology of toxigenic Vibrio cholerae. Microbiol Mol Biol Rev. 1998;62:1301-1314.

    Not in our library10.1128/mmbr.62.4.1301-1314.1998

  22. 22.

    Ferencz A, Orskov I, Orskov F, Klemm P. Deoxyribonucleic acid is a significant component of the small-intestinal mucus. Acta Pathol Microbiol Scand B. 1980;88:347-348.

    Not in our library10.1111/j.1699-0463.1980.tb02654.x

  23. 23.

    Firczuk M, Bochtler M. Folds and activities of peptidoglycan amidases. FEMS Microbiol Rev. 2007;31:676-691.

    Not in our library10.1111/j.1574-6976.2007.00084.x

  24. 24.

    Flemming HC, Wingender J. The biofilm matrix. Nat Rev Microbiol. 2010;8:623-633.

    Not in our library10.1038/nrmicro2415

  25. 25.

    Focareta T, Manning PA. Extracellular proteins of Vibrio cholerae: molecular cloning, nucleotide sequence and characterization of the deoxyribonuclease (DNase) together with its periplasmic localization in Escherichia coli K-12. Gene. 1987;53:31-40.

    Not in our library10.1016/0378-1119(87)90090-4

  26. 26.

    Focareta T, Manning PA. Distinguishing between the extracellular DNases of Vibrio cholerae and development of a transformation system. Mol Microbiol. 1991a;5:2547-2555.

    Not in our library10.1111/j.1365-2958.1991.tb02101.x

  27. 27.

    Focareta T, Manning PA. Genetic analysis of the export of an extracellular DNase of Vibrio cholerae using DNase-beta-lactamase fusions. Gene. 1991b;108:31-37.

    Not in our library10.1016/0378-1119(91)90484-s

  28. 28.

    Fong JC, Syed KA, Klose KE, Yildiz FH. Role of Vibrio polysaccharide (vps) genes in VPS production, biofilm formation and Vibrio cholerae pathogenesis. Microbiology. 2010;156:2757-2769.

    Not in our library10.1099/mic.0.040196-0

  29. 29.

    Freter R, Jones GW. Adhesive properties of Vibrio cholerae: nature of the interaction with intact mucosal surfaces. Infect Immun. 1976;14:246-256.

    Not in our library10.1128/iai.14.1.246-256.1976

  30. 30.

    Freter R, O'Brien PC. Role of chemotaxis in the association of motile bacteria with intestinal mucosa: chemotactic responses of Vibrio cholerae and description of motile nonchemotactic mutants. Infect Immun. 1981;34:215-221.

    Not in our library10.1128/iai.34.1.215-221.1981

  31. 31.

    Freter R, O'Brian PC, Macsai MS. Role of chemotaxis in the association of motile bacteria with intestinal mucosa: in vivo studies. Infect Immun. 1981;34:234-240.

    Not in our library10.1128/iai.34.1.234-240.1981

  32. 32.

    Ghigo JM. Natural conjugative plasmids induce bacterial biofilm development. Nature. 2001;412:442-445.

    Not in our library10.1038/35086581

  33. 33.

    Gilpin RW, Chatterjee AN, Young FE. Autolysis of microbial cells: salt activation of autolytic enzymes in a mutant of Staphylococcus aureus. J Bacteriol. 1972;111:272-283.

    Not in our library10.1128/jb.111.1.272-283.1972

  34. 34.

    Goller CC, Romeo T. Environmental influences on biofilm development. Curr Top Microbiol Immunol. 2008;322:37-66.

    Not in our library10.1007/978-3-540-75418-3_3

  35. 35.

    Grande R, Di Giulio M, Bessa LJ, Di Campli E, Baffoni M, Guarnieri S, Cellini L. Extracellular DNA in Helicobacter pylori biofilm: a backstairs rumour. J Appl Microbiol. 2010;110:490-498.

    Not in our library10.1111/j.1365-2672.2010.04911.x

  36. 36.

    Grimberg J, Maguire S, Belluscio L. A simple method for the preparation of plasmid and chromosomal E. coli DNA. Nucleic Acids Res. 1989;17:8893.

    Not in our library10.1093/nar/17.21.8893

  37. 37.

    Guzman L-M, Beblin D, Carson MJ, Beckwith J. Tight regulation, modulation, and high-level expression by vectors containing the arabinose pBAD promotor. J Bacteriol. 1995;177:4121-4130.

    Not in our library10.1128/jb.177.14.4121-4130.1995

  38. 38.

    Hall-Stoodley L, Stoodley P. Biofilm formation and dispersal and the transmission of human pathogens. Trends Microbiol. 2005;13:7-10.

    Not in our library10.1016/j.tim.2004.11.004

  39. 39.

    Hammer BK, Bassler BL. Quorum sensing controls biofilm formation in Vibrio cholerae. Mol Microbiol. 2003;50:101-104.

    Not in our library10.1046/j.1365-2958.2003.03688.x

  40. 40.

    Hanahan D. Studies on transformation of Escherichia coli with plasmids. J Mol Biol. 1983;166:557-580.

    Not in our library10.1016/s0022-2836(83)80284-8

All 129 references

Cited by papers we hold 17

Reads

Read by people on this page

None yet.

Checked or read by AI through naulon

None yet.

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.

Are you an author?

Is this your paper?

Claim it to add your note and be paid when agents cite it. Free.