A bacterial extracellular DNA inhibits settling of motile progeny cells within a biofilm

Molecular Microbiology

Volumn 77, Issue 4, 2010, Pages 815-829

  Berne, Cécile ^a   Kysela, David T ^a   Brun, Yves V ^a  

^a INDIANA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA;

ARTICLE; BIOFILM; CAULOBACTER CRESCENTUS; CELL ADHESION; CELL DEATH; CELL MOTILITY; CELL SURFACE; CELL SYNCHRONIZATION; CONTROLLED STUDY; DNA BINDING; GENE TARGETING; HYBRID CELL; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; BACTERIUM ADHERENCE; CAULOBACTER VIBRIOIDES; GROWTH, DEVELOPMENT AND AGING; LOCOMOTION; METABOLISM; PHYSIOLOGY;

BACTERIA (MICROORGANISMS); CAULOBACTER VIBRIOIDES; PROTEOBACTERIA;

BACTERIAL ADHESION; BIOFILMS; CAULOBACTER CRESCENTUS; DNA, BACTERIAL; LOCOMOTION;

EID: 77955362784     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2010.07267.x     Document Type: Article

References (53)

1. Ackerley, D.F., Barak, Y., Lynch, S.V., Curtin, J. Matin, A. (2006) Effect of chromate stress on Escherichia coli K-12. J Bacteriol 188 : 3371 3381.
2. Allesen-Holm, M., Barken, K.B., Yang, L., Klausen, M., Webb, J.S., Kjelleberg, S., et al. (2006) A characterization of DNA release in Pseudomonas aeruginosa cultures and biofilms. Mol Microbiol 59 : 1114 1128.
3. Bailey, T.L. Elkan, C. (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf Intell Syst Mol Biol 2 : 28 36.
4. Bailey, T.L. Gribskov, M. (1998) Combining evidence using p-values: application to sequence homology searches. Bioinformatics 14 : 48 54.
5. Bayles, K.W. (2007) The biological role of death and lysis in biofilm development. Nat Rev Microbiol 5 : 721 726.
6. Bodenmiller, D., Toh, E. Brun, Y.V. (2004) Development of surface adhesion in Caulobacter crescentus. J Bacteriol 186 : 1438 1447.
7. Brown, P.J., Hardy, G.G., Trimble, M.J. Brun, Y.V. (2009) Complex regulatory pathways coordinate cell-cycle progression and development in Caulobacter crescentus. Adv Microb Physiol 54 : 1 101.
8. Claverys, J.P. Havarstein, L.S. (2007) Cannibalism and fratricide: mechanisms and raisons d'etre. Nat Rev Microbiol 5 : 219 229.
9. Cole, J.L., Hardy, G.G., Bodenmiller, D., Toh, E., Hinz, A. Brun, Y.V. (2003) The HfaB and HfaD adhesion proteins of Caulobacter crescentus are localized in the stalk. Mol Microbiol 49 : 1671 1683.
10. Davey, M.E. O'Toole, G.A. (2000) Microbial biofilms: from ecology to molecular genetics. Microbiol Mol Biol Rev 64 : 847 867.
11. Degnen, S.T. Newton, A. (1972) Chromosome replication during development in Caulobacter crescentus. J Mol Biol 64 : 671 680.
12. Entcheva-Dimitrov, P. Spormann, A.M. (2004) Dynamics and control of biofilms of the oligotrophic bacterium Caulobacter crescentus. J Bacteriol 186 : 8254 8266.
13. Evinger, M. Agabian, N. (1977) Envelope-associated nucleoid from Caulobacter crescentus stalked and swarmer cells. J Bacteriol 132 : 294 301.
14. Goller, C.C. Romeo, T. (2008) Environmental influences on biofilm development. Curr Top Microbiol Immunol 322 : 37 66.
15. Hall-Stoodley, L., Costerton, J.W. Stoodley, P. (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2 : 95 108.
16. Hardy, G.G., Allen, R.C., Toh, E., Long, M., Cole, J.L. Brun, Y.V. (2010) A localized multimeric anchor attaches the Caulobacter holdfast to the cell pole. Mol Microbiol 76 : 409 427.
17. Harrison, J.J., Ceri, H. Turner, R.J. (2007) Multimetal resistance and tolerance in microbial biofilms. Nat Rev Microbiol 5 : 928 938.
18. Johnson, R.C. Ely, B. (1977) Isolation of spontaneously derived mutants of Caulobacter crescentus. Genetics 86 : 25 32. (Pubitemid 8127921)
19. Jurcisek, J.A. Bakaletz, L.O. (2007) Biofilms formed by nontypeable Haemophilus influenzae in vivo contain both double-stranded DNA and type IV pilin protein. J Bacteriol 189 : 3868 3875.
20. Karatan, E. Watnick, P. (2009) Signals, regulatory networks, and materials that build and break bacterial biofilms. Microbiol Mol Biol Rev 73 : 310 347.
21. Kolter, R. Greenberg, E.P. (2006) Microbial sciences: the superficial life of microbes. Nature 441 : 300 302.
22. Kurtz, H.D., Jr. Smith, J. (1992) Analysis of a Caulobacter crescentus gene cluster involved in attachment of the holdfast to the cell. J Bacteriol 174 : 687 694.
23. Lagenaur, C. Agabian, N. (1977) Caulobacter flagellins. J Bacteriol 132 : 731 733.
24. Lappann, M., Claus, H., van Alen, T., Harmsen, M., Elias, J., Molin, S. Vogel, U. (2010) A dual role of extracellular DNA during biofilm formation of Neisseria meningitidis. Mol Microbiol 75 : 1355 1371.
25. Larimer, F.W., Chain, P., Hauser, L., Lamerdin, J., Malfatti, S., Do, L., et al. (2004) Complete genome sequence of the metabolically versatile photosynthetic bacterium Rhodopseudomonas palustris. Nat Biotechnol 22 : 55 61.
26. Larson, R.J. Pate, J.L. (1975) Growth and morphology of Asticcacaulis biprosthecum in defined media. Arch Microbiol 106 : 147 157.
27. Levi, A. Jenal, U. (2006) Holdfast formation in motile swarmer cells optimizes surface attachment during Caulobacter crescentus development. J Bacteriol 188 : 5315 5318.
28. Lopez, D., Vlamakis, H., Losick, R. Kolter, R. (2009) Cannibalism enhances biofilm development in Bacillus subtilis. Mol Microbiol 74 : 609 618.
29. Lorenz, M.G. Wackernagel, W. (1994) Bacterial gene transfer by natural genetic transformation in the environment. Microbiol Rev 58 : 563 602.
30. Mannisto, M.K., Tiirola, M.A., Salkinoja-Salonen, M.S., Kulomaa, M.S. Puhakka, J.A. (1999) Diversity of chlorophenol-degrading bacteria isolated from contaminated boreal groundwater. Arch Microbiol 171 : 189 197.
31. Meade, H.M., Long, S.R., Ruvkun, G.B., Brown, S.E. Ausubel, F.M. (1982) Physical and genetic characterization of symbiotic and auxotrophic mutants of Rhizobium meliloti induced by transposon Tn5 mutagenesis. J Bacteriol 149 : 114 122.
32. Merker, R.I. Smit, J. (1988) Characterization of the Adhesive Holdfast of Marine and Freshwater Caulobacters. Appl Environ Microbiol 54 : 2078 2085.
33. Merritt, P.M., Danhorn, T. Fuqua, C. (2007) Motility and chemotaxis in Agrobacterium tumefaciens surface attachment and biofilm formation. J Bacteriol 189 : 8005 8014.
34. Meyers, L.A. Bull, J.J. (2002) Fighting change with change: adaptive variation in an uncertain world. Trends Ecol Evol 17 : 551 557.
35. Moons, P., Michiels, C.W. Aertsen, A. (2009) Bacterial interactions in biofilms. Crit Rev Microbiol 35 : 157 168.
36. Nadell, C.D., Xavier, J.B. Foster, K.R. (2009) The sociobiology of biofilms. FEMS Microbiol Rev 33 : 206 224.
37. Pate, J.L. Ordal, E.J. (1965) The fine structure of two unusual stalked bacteria. J Cell Biol 27 : 133 150.
38. Poindexter, J.S. (1964) Biological properties and classification of the caulobacter group. Bacteriol Rev 28 : 231 295.
39. Rice, K.C. Bayles, K.W. (2008) Molecular control of bacterial death and lysis. Microbiol Mol Biol Rev 72 : 85 109.
40. Sakurai, K., Uezu, K., Numata, M., Hasegawa, T., Li, C., Kaneko, K. Shinkai, S. (2005) Beta-1,3-glucan polysaccharides as novel one-dimensional hosts for DNA/RNA, conjugated polymers and nanoparticles. Chem Commun (Camb) 35 : 4383 4398.
41. Schooling, S.R. Beveridge, T.J. (2006) Membrane vesicles: an overlooked component of the matrices of biofilms. J Bacteriol 188 : 5945 5957.
42. Smit, J. Agabian, N. (1984) Cloning of the major protein of the Caulobacter crescentus periodic surface layer: detection and characterization of the cloned peptide by protein expression assays. J Bacteriol 160 : 1137 1145.
43. Spoering, A.L. Gilmore, M.S. (2006) Quorum sensing and DNA release in bacterial biofilms. Curr Opin Microbiol 9 : 133 137.
44. Spormann, A.M. (2008) Physiology of microbes in biofilms. Curr Top Microbiol Immunol 322 : 17 36.
45. Stephens, C., Reisenauer, A., Wright, R. Shapiro, L. (1996) A cell cycle-regulated bacterial DNA methyltransferase is essential for viability. Proc Natl Acad Sci USA 93 : 1210 1214.
46. Stewart, P.S. Franklin, M.J. (2008) Physiological heterogeneity in biofilms. Nat Rev Microbiol 6 : 199 210.
47. Swofford, D.L. (2003) PAUP*. Phylogenetic Analysis Using Parsimony (* and Other Methods). Sunderland, MA : Sinauer Associates.
48. Tart, A.H. Wozniak, D.J. (2008) Shifting paradigms in Pseudomonas aeruginosa biofilm research. Curr Top Microbiol Immunol 322 : 193 206.
49. Thomas, V.C., Hiromasa, Y., Harms, N., Thurlow, L., Tomich, J. Hancock, L.E. (2009) A fratricidal mechanism is responsible for eDNA release and contributes to biofilm development of Enterococcus faecalis. Mol Microbiol 72 : 1022 1036.
50. Tsang, P.H., Li, G., Brun, Y.V., Freund, L.B. Tang, J.X. (2006) Adhesion of single bacterial cells in the micronewton range. Proc Natl Acad Sci USA 103 : 5764 5768.
51. Watson, B., Currier, T.C., Gordon, M.P., Chilton, M.D. Nester, E.W. (1975) Plasmid required for virulence of Agrobacterium tumefaciens. J Bacteriol 123 : 255 264.
52. West, L., Yang, D. Stephens, C. (2002) Use of the Caulobacter crescentus genome sequence to develop a method for systematic genetic mapping. J Bacteriol 184 : 2155 2166.
53. Whitchurch, C.B., Tolker-Nielsen, T., Ragas, P.C. Mattick, J.S. (2002) Extracellular DNA required for bacterial biofilm formation. Science 295 : 1487.