The spatial architecture of Bacillus subtilis biofilms deciphered using a surface-associated model and in Situ imaging

PLoS ONE

Volumn 6, Issue 1, 2011, Pages

  Bridier, Arnaud ^a   Le Coq, Dominique ^a   Dubois Brissonnet, Florence ^a   Thomas, Vincent ^b   Aymerich, Stéphane ^a   Briandet, Romain ^a  

^a UMR1319 MICALIS   (France)

^b Steris   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL CELL; BACTERIAL STRAIN; BACTERIUM CULTURE; BIOFILM; CELL ADHESION; CELL COUNT; COLONY FORMATION; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; GENE IDENTIFICATION; GENOTYPE; MUTATION; NONHUMAN; PHENOTYPE; CONFOCAL MICROSCOPY; GENETICS; GROWTH, DEVELOPMENT AND AGING; SURFACE PROPERTY;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); POSIBACTERIA;

BACILLUS SUBTILIS; BIOFILMS; MICROSCOPY, CONFOCAL; MUTATION; SURFACE PROPERTIES;

EID: 79251563218     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0016177     Document Type: Article

References (56)

1. Costerton JW (1995) Overview of microbial biofilms. J Ind Microbiol 15: 137-140.
2. Kolter R, Greenberg EP (2006) The superficial life of microbes. Nature 441: 300-302.
3. Watnick P, Kolter R (2000) Biofilm, city of microbes. J Bacteriol 182: 2675-2679.
4. Costerton JW (2007) The biofilm primer. Springer series on biofilms. pp 5-6.
5. Singh R, Debarati P, Rakesh KJ (2006) Biofilms, implications in bioremediation. Trends Microbiol 14: 389-397.
6. Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms, a common cause of persistent infections. Science 284: 1318-1322.
7. Hall-stoodley L, Stoodley P (2009) Evolving concepts in biofilm infections. Cell Microbiol 11: 1034-1043.
8. Potera C (1999) Forging a link between biofilms and disease. Science 283: 1837-1839.
9. Lemon KP, Earl AM, Vlamakis HC, Aguilar C, Kolter R (2008) Biofilm development with an emphasis on Bacillus subtilis. Curr Top Microbiol Immunol 322: 1-16.
10. Branda SS, Gonzalez-Pastor JE, Ben-Yehuda S, Losick R, Kolter R (2001) Fruiting body formation by Bacillus subtilis. Proc Natl Acad Sci USA 98: 11621-11626.
11. Kobayashi K (2007) Bacillus subtilis pellicle formation proceeds through genetically defined morphological changes. J Bacteriol 189: 4920-4931.
12. Blair KM, Turner L, Winkelman JT, Berg HC, Kearns DB (2008) A molecular clutch disables flagella in the Bacillus subtilis biofilm. Science 320: 1636-1638.
13. Branda SS, Chu F, Kearns DB, Losick R, Kolter R (2006) A major protein component of the Bacillus subtilis biofilm matrix. Mol Microbiol 59: 1229-1238.
14. Chu F, Kearns DB, Branda SS, Kolter R, Losick R (2006) Targets of the master regulator of biofilm formation in Bacillus subtilis. Mol Microbiol 59: 1216-1228.
15. Romero D, Aguilar C, Losick R, Kolter R (2010) Amyloid fibers provide structural integrity to Bacillus subtilis biofilms. Proc Natl Acad Sci USA 107: 2230-2234.
16. Chai Y, Kolter R, Losick R (2009) Paralogous antirepressors acting on the master regulator for biofilm formation in Bacillus subtilis. Mol Microbiol 74: 876-887.
17. Hamon MA, Lazazzera BA (2001) The sporulation transcription factor Spo0A is required for biofilm development in Bacillus subtilis. Mol Microbiol 42: 1199-1209.
18. Hamon MA, Stanley NR, Britton RA, Grossman AD, Lazazzera BA (2004) Identification of AbrB-regulated genes involved in biofilm formation by Bacillus subtilis. Mol Microbiol 52: 847-860.
19. Kearns DB, Chu F, Branda SS, Kolter R, Losick R (2005) A master regulator for biofilm formation by Bacillus subtilis. Mol Microbiol 55: 739-749.
20. Kobayashi K (2008) SlrR/SlrA controls the initiation of biofilm formation in Bacillus subtilis. Mol Microbiol 69: 1399-1410.
21. Murray EJ, Kiley TB, Stanley-Wall NR (2009) A pivotal role for the response regulator DegU in controlling multicellular behaviour. Microbiology 155: 1-8.
22. Verhamme DT, Murray EJ, Stanley-Wall NR (2009) DegU and Spo0A jointly control transcription of two loci required for complex colony development by Bacillus subtilis. J Bacteriol 191: 100-108.
23. Chai Y, Chu F, Kolter R, Losick R (2008) Bistability and biofilm formation in Bacillus subtilis. Mol Microbiol 67: 254-263.
24. Fujita M, Gonzalez-Pastor JE, Losick R (2005) High- and low-threshold genes in the Spo0A regulon of Bacillus subtilis. J Bacteriol 187: 1357-1368.
25. Chai Y, Norman T, Kolter R, Losick R (2010) An epigenetic switch governing daughter cell separation in Bacillus subtilis. Genes Dev 24: 754-765.
26. Chu F, Kearns DB, McLoon A, Chai Y, Kolter R, et al. (2008) A novel regulatory protein governing biofilm biofilm formation in Bacillus subtilis. Mol Microbiol 68: 1117-1127.
27. Kobayashi K (2007) Gradual activation of the global response regulator DegU controls serial expression of genes for flagellum formation and biofilm formation in Bacillus subtilis. Mol Microbiol 66: 395-409.
28. Stanley NR, Lazazzera BA (2005) Defining the genetic differences between wild and domestic strains of Bacillus subtilis that affect poly-gamma-DL-glutamic acid production and biofilm formation. Mol Microbiol 57: 1143-1158.
29. Verhamme DT, Kiley TB, Stanley-Wall NR (2007) DegU co-ordinates multicellular behaviour exhibited by Bacillus subtilis. Mol Microbiol 65: 554-568.
30. Stanley NR, Britton RA, Grossman AD, Lazazzera BA (2003) Identification of catabolite repression as a physiological regulator of biofilm formation by Bacillus subtilis by use of DNA microarrays. J Bacteriol 185: 1951-1957.
31. Jules M, Le Chat L, Aymerich S, Le Coq D (2009) The Bacillus subtilis ywjI (glpX) gene encodes a Class II Fructose-1, 6-Bisphosphatase, functionally equivalent to the Class III Fbp enzyme. J Bacteriol 191: 3168-3171.
32. Bridier A, Dubois-Brissonnet F, Boubetra A, Thomas V, Briandet R (2010) The biofilm architecture of sixty opportunistics pathogens deciphered using a high throughput CLSM method. J Microbiol Methods 82: 64-70.
33. Xavier JB, White DC, Almeida JS (2003) Automated biofilm morphology quantification from confocal laser scanning microscopy imaging. Wat Sci Tech 47: 31-37.
34. Kuehn M, Hausner M, Bungartz HJ, Wagner M, Wilderer PA, et al. (1998) Automated confocal laser scanning microscopy and semiautomated image processing for analysis of biofilms. Appl Environ Microbiol 64: 4115-4127.
35. Martin DJH, Denyer SP, McDonnell G, Maillard JY (2008) Resistance and cross-resistance to oxidising agents of bacterial isolates from endoscope washer disinfectors. J Hosp Infect 69: 377-383.
36. Barken KB, Pamp SJ, Yang L, Gjermansen M, Bertrand JJ, et al. (2008) Roles of type IV pili, flagellum-mediated motility and extracellular DNA in the formation of mature multicellular structures in Pseudomonas aeruginosa biofilms. Environ Microbiol 10: 2331-2343.
37. Houry A, Briandet R, Aymerich S, Gohar M (2010) Motility and flagellum involvement in Bacillus cereus biofilm formation. Microbiol 156: 1009-1018.
38. Lemon KP, Higgins DE, Kolter R (2007) Flagellar is critical for Listeria monocytogenes biofilm formation. J Bacteriol 189: 4418-4424.
39. Wood TK, Gonzalez Barrios AF, Herzberg M, Lee J (2006) Motility influences biofilms architecture in Escherichia coli. Appl Microbiol Biotechnol 72: 361-367.
40. Branda SS, Gonzalez-Pastor JE, Dervyn E, Ehrlich D, Losick R, et al. (2004) Genes involved in formation of structured multicellular communities by Bacillus subtilis. J Bacteriol 186: 3970-3979.
41. Ohsawa T, Tsukahara K, Ogura M (2009) Bacillus subtilis response regulator DegU is a direct activator of pgsB transcription involved in gamma-polyglutamic acid synthesis. Biosci Biotechnol Biochem 73: 2096-2102.
42. Dahl MK, Msadek T, Kunst F, Rapaport G (1992) The phosphorylation state of the DegU response regulator acts as a molecular switch allowing either degradative enzyme synthesis or expression of genetic competence in Bacillus subtilis. J Biol Chem 267: 14509-14514.
43. Amati G, Bisicchia P, Galizzi A (2004) DegU-P represses expression of the motility fla-che operon in Bacillus subtilis. J Bacteriol 186: 6003-6014.
44. B control, on biofilm formation. J Bacteriol 190: 3546-3556.
45. Kolodkin-Gal I, Romero D, Cao S, Clardy J, Kolter R, et al. (2010) D-amino acids trigger biofilm disassembly. Science 328: 627-629.
46. Stöver AG, Driks A (1999) Control of synthesis and secretion of the Bacillus subtilis protein YqxM. J Bacteriol 181: 7065-7069.
47. Jonas K, Tomenius H, Kader A, Normak S, Römling U, et al. (2007) Roles of curli, cellulose and BapA in Salmonella biofilm morphology studied by atomic force microscopy. BMC Microbiol 7: 70.
48. Prigent-Combaret C, Prensier G, Le Thi TT, Vidal O, Lejeune P, et al. (2000) Developmental pathway for biofilm formation in curli-producing Escherichia coli strains: role of flagella, curli and colanic acid. Environ Microbiol 2: 450-464.
49. Ryu JH, Beuchat LR (2005) Biofilm formation by Escherichia coli 0157:H7 on stainless steel: Effect of exopolysaccharide and Curli production on its resistance to chlorine. Appl Environ Microbiol 71: 247-254.
50. Watnick PI, Lauriano CM, Klose KE, Croal L, Kolter R (2001) The absence of a flagellum leads to altered colony morphology, biofilm development and virulence in Vibrio Cholerae 0139. Mol Microbiol 39: 223-235.
51. Yang M, Shimotsu H, Ferrari E, Henner DJ (1987) Characterization and mapping of the Bacillus subtilis prtR gene. J Bacteriol 169: 434-437.
52. Crutz AM, Steinmetz M (1992) Transcription of the Bacillus subtilis sacX and sacY genes, encoding regulators of sucrose metabolism, is both inducible by sucrose and controlled by the DegS-DegU signalling system. J Bacteriol 174: 6087-6095.
53. Kiel JAKW, Ten Berge AM, Borger P, Venema G (1995) A general method for the consecutive integration of single copies of a heterologous gene at multiple locations in the Bacillus subtilis chromosome by replacement recombination. Appl Env Microbiol 61: 4244-4250.
54. Baptista C, Santos MA, São-José C (2008) Phage SPP1 reversible adsorption to Bacillus subtilis cell wall teichoic acids accelerates virus recognition of membrane receptor YueB. J Bacteriol 190: 4989-4996.
55. Hamze K, Julkowska D, Autret S, Hinc K, Nagorska K, et al. (2009) Identification of genes required for different stages of dendritic swarming in Bacillus subtilis, with a novel role for phrC. Microbiol 155: 398-412.
56. Kobayashi K, Ehrlich SD, Albertini A, Amati G, Andersen KK, et al. (2003) Essential Bacillus subtilis genes. Proc Natl Acad Sci USA 100: 4678-4683.