Biofilm formation by Bacillus subtilis: New insights into regulatory strategies and assembly mechanisms

Molecular Microbiology

Volumn 93, Issue 4, 2014, Pages 587-598

  Cairns, Lynne S ^a   Hobley, Laura ^a   Stanley Wall, Nicola R ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROPHOBIN; POLYSACCHARIDE; PROTEIN SINR; PROTEIN SPO0A; PROTEIN TASA; SCLEROPROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; BACTERIAL DNA; BACTERIAL PROTEIN;

BACILLUS SUBTILIS; BACTERIAL FLAGELLUM; BIOFILM; BIOSYNTHESIS; CELL DEATH; CELL DENSITY; CELL DIFFERENTIATION; CHEMICAL COMPOSITION; EXTRACELLULAR MATRIX; GENE EXPRESSION; GENETIC TRANSCRIPTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; REVIEW; ROTATION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGY;

BACILLUS SUBTILIS; POSIBACTERIA;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; BIOFILMS; DNA, BACTERIAL; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION, BACTERIAL;

EID: 84925884632     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12697     Document Type: Review

References (88)

1. Asally, M., Kittisopikul, M., Rue, P., Du, Y., Hu, Z., Cagatay, T., etal. (2012) Localized cell death focuses mechanical forces during 3D patterning in a biofilm. Proc Natl Acad Sci USA 109: 18891-18896.
2. Bai, U., Mandic-Mulec, I., and Smith, I. (1993) SinI modulates the activity of SinR, a developmental switch protein of Bacillus subtilis, by protein-protein interaction. Genes Dev 7: 139-148.
3. Bais, H.P., Fall, R., and Vivanco, J.M. (2004) Biocontrol of Bacillus subtilis against infection of Arabidopsis roots by Pseudomonas syringae is facilitated by biofilm formation and surfactin production. Plant Physiol 134: 307-319.
4. Banse, A.V., Chastanet, A., Rahn-Lee, L., Hobbs, E.C., and Losick, R. (2008) Parallel pathways of repression and antirepression governing the transition to stationary phase in Bacillus subtilis. Proc Natl Acad Sci USA 105: 15547-15552.
5. Beauregard, P.B., Chai, Y., Vlamakis, H., Losick, R., and Kolter, R. (2013) Bacillus subtilis biofilm induction by plant polysaccharides. Proc Natl Acad Sci USA 110: E1621-E1630.
6. Benigar, E., Dogsa, I., Stopar, D., Jamnik, A., Kralj Cigic, I., and Tomsic, M. (2014) Structure and dynamics of a polysaccharide matrix: aqueous solutions of bacterial levan. Langmuir 30: 4172-4182.
7. Blair, K.M., Turner, L., Winkelman, J.T., Berg, H.C., and Kearns, D.B. (2008) A molecular clutch disables flagella in the Bacillus subtilis biofilm. Science 320: 1636-1638.
8. Branda, S.S., Gonzalez-Pastor, J.E., Ben-Yehuda, S., Losick, R., and Kolter, R. (2001) Fruiting body formation by Bacillus subtilis. Proc Natl Acad Sci USA 98: 11621-11626.
9. Branda, S.S., Vik, S., Friedman, L., and Kolter, R. (2005) Biofilms: the matrix revisited. Trends Microbiol 13: 20-26.
10. Branda, S.S., Chu, F., Kearns, D.B., Losick, R., and Kolter, R. (2006) A major protein component of the Bacillus subtilis biofilm matrix. Mol Microbiol 59: 1229-1238.
11. Burrell, M., Hanfrey, C.C., Murray, E.J., Stanley-Wall, N.R., and Michael, A.J. (2010) Evolution and multiplicity of arginine decarboxylases in polyamine biosynthesis and essential role in Bacillus subtilis biofilm formation. J Biol Chem 285: 39224-39238.
12. Cairns, L.S., Marlow, V.L., Bissett, E., Ostrowski, A., and Stanley-Wall, N.R. (2013) A mechanical signal transmitted by the flagellum controls signalling in Bacillus subtilis. Mol Microbiol 90: 6-21.
13. Chai, L., Romero, D., Kayatekin, C., Akabayov, B., Vlamakis, H., Losick, R., and Kolter, R. (2013) Isolation, characterization, and aggregation of a structured bacterial matrix precursor. J Biol Chem 288: 17559-17568.
14. Chai, Y., Chu, F., Kolter, R., and Losick, R. (2008) Bistability and biofilm formation in Bacillus subtilis. Mol Microbiol 67: 254-263.
15. Chai, Y., Kolter, R., and Losick, R. (2009) Paralogous antirepressors acting on the master regulator for biofilm formation in Bacillus subtilis. Mol Microbiol 74: 876-887.
16. Chai, Y., Kolter, R., and Losick, R. (2010a) Reversal of an epigenetic switch governing cell chaining in Bacillus subtilis by protein instability. Mol Microbiol 78: 218-229.
17. Chai, Y., Norman, T., Kolter, R., and Losick, R. (2010b) An epigenetic switch governing daughter cell separation in Bacillus subtilis. Genes Dev 24: 754-765.
18. Chai, Y., Norman, T., Kolter, R., and Losick, R. (2010c) An epigenetic switch governing daughter cell separation in Bacillus subtilis. Genes Dev 24: 754-765.
19. Chai, Y., Beauregard, P.B., Vlamakis, H., Losick, R., and Kolter, R. (2012) Galactose metabolism plays a crucial role in biofilm formation by Bacillus subtilis. mBio 3: e184-e112.
20. Chan, J.M., Guttenplan, S.B., and Kearns, D.B. (2014) Defects in the flagellar motor increase synthesis of poly-gamma-glutamate in Bacillus subtilis. J Bacteriol 196: 740-753.
21. Chen, Y., Cao, S., Chai, Y., Clardy, J., Kolter, R., Guo, J.H., and Losick, R. (2012) A Bacillus subtilis sensor kinase involved in triggering biofilm formation on the roots of tomato plants. Mol Microbiol 85: 418-430.
22. Chen, Y., Yan, F., Chai, Y., Liu, H., Kolter, R., Losick, R., and Guo, J.H. (2013) Biocontrol of tomato wilt disease by Bacillus subtilis isolates from natural environments depends on conserved genes mediating biofilm formation. Environ Microbiol 15: 848-864.
23. Chu, F., Kearns, D.B., McLoon, A., Chai, Y., Kolter, R., and Losick, R. (2008) A novel regulatory protein governing biofilm formation in Bacillus subtilis. Mol Microbiol 68: 1117-1127.
24. Chumsakul, O., Takahashi, H., Oshima, T., Hishimoto, T., Kanaya, S., Ogasawara, N., and Ishikawa, S. (2011) Genome-wide binding profiles of the Bacillus subtilis transition state regulator AbrB and its homolog Abh reveals their interactive role in transcriptional regulation. Nucleic Acids Res 39: 414-428.
25. Costerton, J.W., Lewandowski, Z., Caldwell, D.E., Korber, D.R., and Lappin-Scott, H.M. (1995) Microbial biofilms. Annu Rev Microbiol 49: 711-745.
26. Dogsa, I., Brloznik, M., Stopar, D., and Mandic-Mulec, I. (2013) Exopolymer diversity and the role of levan in Bacillus subtilis biofilms. PLoS ONE 8: e62044.
27. Elliot, M.A., and Talbot, N.J. (2004) Building filaments in the air: aerial morphogenesis in bacteria and fungi. Curr Opin Microbiol 7: 594-601.
28. Elsholz, A.K., Turgay, K., Michalik, S., Hessling, B., Gronau, K., Oertel, D., etal. (2012) Global impact of protein arginine phosphorylation on the physiology of Bacillus subtilis. Proc Natl Acad Sci USA 109: 7451-7456.
29. Epstein, A.K., Pokroy, B., Seminara, A., and Aizenberg, J. (2011) Bacterial biofilm shows persistent resistance to liquid wetting and gas penetration. Proc Natl Acad Sci USA 108: 995-1000.
30. Fagerlund, A., Dubois, T., Okstad, O.A., Verplaetse, E., Gilois, N., Bennaceur, I., etal. (2014) SinR controls enterotoxin expression in Bacillus thuringiensis biofilms. PLoS ONE 9: e87532.
31. Fraser, P.E., Nguyen, J.T., Surewicz, W.K., and Kirschner, D.A. (1991) pH-dependent structural transitions of Alzheimer amyloid peptides. Biophys J 60: 1190-1201.
32. Fujita, M., Gonzalez-Pastor, J.E., and Losick, R. (2005) High- and low-threshold genes in the Spo0A regulon of Bacillus subtilis. J Bacteriol 187: 1357-1368.
33. Gerwig, J., Kiley, T.B., Gunka, K., Stanley-Wall, N., and Stulke, J. (2014) The protein tyrosine kinases EpsB and PtkA differentially affect biofilm formation in Bacillus subtilis. Microbiology 160 (Pt 4): 682-691.
34. Guttenplan, S.B., Blair, K.M., and Kearns, D.B. (2010) The EpsE flagellar clutch is bifunctional and synergizes with EPS biosynthesis to promote Bacillus subtilis biofilm formation. PLoS Genet 6: e1001243.
35. Halan, B., Buehler, K., and Schmid, A. (2012) Biofilms as living catalysts in continuous chemical syntheses. Trends Biotechnol 30: 453-465.
36. Hall, M.R., McGillicuddy, E., and Kaplan, L.J. (2014) Biofilm: basic principles, pathophysiology, and implications for clinicians. Surg Infect 15: 1-7.
37. Hamon, M.A., and Lazazzera, B.A. (2001) The sporulation transcription factor Spo0A is required for biofilm development in Bacillus subtilis. Mol Microbiol 42: 1199-1209.
38. Hamon, M.A., Stanley, N.R., Britton, R.A., Grossman, A.D., and Lazazzera, B.A. (2004) Identification of AbrB-regulated genes involved in biofilm formation by Bacillus subtilis. Mol Microbiol 52: 847-860.
39. Hobley, L., Ostrowski, A., Rao, F.V., Bromley, K.M., Porter, M., Prescott, A.R., etal. (2013) BslA is a self-assembling bacterial hydrophobin that coats the Bacillus subtilis biofilm. Proc Natl Acad Sci USA 110: 13600-13605.
40. Hobley, L., Kim, S.H., Maezato, Y., Wyllie, S., Fairlamb, A.H., Stanley-Wall, N.R., and Michael, A.J. (2014) Norspermidine is not a self-produced trigger for biofilm disassembly. Cell 156: 844-854.
41. Hsu, R.L., Lee, K.T., Wang, J.H., Lee, L.Y., and Chen, R.P. (2009) Amyloid-degrading ability of nattokinase from Bacillus subtilis natto. J Agric Food Chem 57: 503-508.
42. Jones, S.E., Paynich, M.L., Kearns, D.B., and Knight, K.L. (2014) Protection from intestinal inflammation by bacterial exopolysaccharides. J Immunol 192: 4813-4820.
43. Kearns, D.B., Chu, F., Branda, S.S., Kolter, R., and Losick, R. (2005) A master regulator for biofilm formation by Bacillus subtilis. Mol Microbiol 55: 739-749.
44. Kiley, T.B., and Stanley-Wall, N.R. (2010) Post-translational control of Bacillus subtilis biofilm formation mediated by tyrosine phosphorylation. Mol Microbiol 78: 947-963.
45. Kobayashi, K. (2007) Gradual activation of the response regulator DegU controls serial expression of genes for flagellum formation and biofilm formation in Bacillus subtilis. Mol Microbiol 66: 395-409.
46. Kobayashi, K. (2008) SlrR/SlrA controls the initiation of biofilm formation in Bacillus subtilis. Mol Microbiol 69: 1399-1410.
47. Kobayashi, K., and Iwano, M. (2012) BslA (YuaB) forms a hydrophobic layer on the surface of Bacillus subtilis biofilms. Mol Microbiol 85: 51-66.
48. Kolodkin-Gal, I., Romero, D., Cao, S., Clardy, J., Kolter, R., and Losick, R. (2010) d-amino acids trigger biofilm disassembly. Science 328: 627-629.
49. Kolodkin-Gal, I., Cao, S., Chai, L., Bottcher, T., Kolter, R., Clardy, J., and Losick, R. (2012) A self-produced trigger for biofilm disassembly that targets exopolysaccharide. Cell 149: 684-692.
50. Leiman, S.A., May, J.M., Lebar, M.D., Kahne, D., Kolter, R., and Losick, R. (2013) d-amino acids indirectly inhibit biofilm formation in Bacillus subtilis by interfering with protein synthesis. J Bacteriol 195: 5391-5395.
51. Levine, A., Vannier, F., Absalon, C., Kuhn, L., Jackson, P., Scrivener, E., etal. (2006) Analysis of the dynamic Bacillus subtilis Ser/Thr/Tyr phosphoproteome implicated in a wide variety of cellular processes. Proteomics 6: 2157-2173.
52. Lewis, R.J., Brannigan, J.A., Offen, W.A., Smith, I., and Wilkinson, A.J. (1998) An evolutionary link between sporulation and prophage induction in the structure of a repressor:anti-repressor complex. J Mol Biol 283: 907-912.
53. Little, J.W. (1984) Autodigestion of lexA and phage lambda repressors. Proc Natl Acad Sci USA 81: 1375-1379.
54. Liu, Y., Zhang, W., Sileika, T., Warta, R., Cianciotto, N.P., and Packman, A. (2009) Role of bacterial adhesion in the microbial ecology of biofilms in cooling tower systems. Biofouling 25: 241-253.
55. Lopez, D., and Kolter, R. (2010) Extracellular signals that define distinct and coexisting cell fates in Bacillus subtilis. FEMS Microbiol Rev 34: 134-149.
56. Lopez, D., Vlamakis, H., and Kolter, R. (2009) Generation of multiple cell types in Bacillus subtilis. FEMS Microbiol Rev 33: 152-163.
57. Macek, B., Mijakovic, I., Olsen, J.V., Gnad, F., Kumar, C., Jensen, P.R., and Mann, M. (2007) The serine/threonine/tyrosine phosphoproteome of the model bacterium Bacillus subtilis. Mol Cell Proteomics 6: 697-707.
58. Marlow, V.L., Cianfanelli, F.R., Porter, M., Cairns, L.S., Dale, J.K., and Stanley-Wall, N.R. (2014a) The prevalence and origin of exoprotease-producing cells in the Bacillus subtilis biofilm. Microbiology 160: 56-66.
59. Marlow, V.L., Porter, M., Hobley, L., Kiley, T.B., Swedlow, J.R., Davidson, F.A., and Stanley-Wall, N.R. (2014b) Phosphorylated DegU manipulates cell fate differentiation in the Bacillus subtilis biofilm. J Bacteriol 196: 16-27.
60. Mukai, K., Kawata, M., and Tanaka, T. (1990) Isolation and phosphorylation of the Bacillus subtilis degS and degU gene products. J Biol Chem 265: 20000-20006.
61. Murray, E.J., Kiley, T.B., and Stanley-Wall, N.R. (2009a) A pivotal role for the response regulator DegU in controlling multicellular behaviour. Microbiology 155: 1-8.
62. Murray, E.J., Strauch, M.A., and Stanley-Wall, N.R. (2009b) σX is involved in controlling Bacillus subtilis biofilm architecture through the AbrB homologue Abh. J Bacteriol 191: 6822-6832.
63. Newman, J.A., and Lewis, R.J. (2013) Exploring the role of SlrR and SlrA in the SinR epigenetic switch. Commun Integr Biol 6: e25658.
64. Newman, J.A., Rodrigues, C., and Lewis, R.J. (2013) Molecular basis of the activity of SinR protein, the master regulator of biofilm formation in Bacillus subtilis. J Biol Chem 288: 10766-10778.
65. Norman, T.M., Lord, N.D., Paulsson, J., and Losick, R. (2013) Memory and modularity in cell-fate decision making. Nature 503: 481-486.
66. Ostrowski, A., Mehert, A., Prescott, A., Kiley, T.B., and Stanley-Wall, N.R. (2011) YuaB functions synergistically with the exopolysaccharide and TasA amyloid fibers to allow biofilm formation by Bacillus subtilis. J Bacteriol 193: 4821-4831.
67. Romero, D., Aguilar, C., Losick, R., and Kolter, R. (2010) Amyloid fibers provide structural integrity to Bacillus subtilis biofilms. Proc Natl Acad Sci USA 107: 2230-2234.
68. Romero, D., Vlamakis, H., Losick, R., and Kolter, R. (2011) An accessory protein required for anchoring and assembly of amyloid fibres in B. subtilis biofilms. Mol Microbiol 80: 1155-1168.
69. Romero, D., Vlamakis, H., Losick, R., and Kolter, R. (2014) Functional analysis of the accessory protein TapA in Bacillus subtilis amyloid fiber assembly. J Bacteriol 196: 1505-1513.
70. Scott, D.J., Leejeerajumnean, S., Brannigan, J.A., Lewis, R.J., Wilkinson, A.J., and Hoggett, J.G. (1999) Quaternary re-arrangement analysed by spectral enhancement: the interaction of a sporulation repressor with its antagonist. J Mol Biol 293: 997-1004.
71. Seminara, A., Angelini, T.E., Wilking, J.N., Vlamakis, H., Ebrahim, S., Kolter, R., etal. (2012) Osmotic spreading of Bacillus subtilis biofilms driven by an extracellular matrix. Proc Natl Acad Sci USA 109: 1116-1121.
72. Sokolowski, F., Modler, A.J., Masuch, R., Zirwer, D., Baier, M., Lutsch, G., etal. (2003) Formation of critical oligomers is a key event during conformational transition of recombinant Syrian hamster prion protein. J Biol Chem 278: 40481-40492.
73. Soutourina, O., Soutourina, J., Blanquet, S., and Plateau, P. (2004) Formation of d-tyrosyl-tRNATyr accounts for the toxicity of d-tyrosine toward Escherichia coli. J Biol Chem 279: 42560-42565.
74. Stover, A.G., and Driks, A. (1999) Secretion. localization and antibacterial activity of tasA, a Bacillus subtilis spore-associated protein. J Bacteriol 181: 1664-1672.
75. Strauch, M., Webb, V., Spiegelman, G., and Hoch, J.A. (1990) The SpoOA protein of Bacillus subtilis is a repressor of the abrB gene. Proc Natl Acad Sci USA 87: 1801-1805.
76. Subramaniam, A.R., Deloughery, A., Bradshaw, N., Chen, Y., O'Shea, E., Losick, R., and Chai, Y. (2013) A serine sensor for multicellularity in a bacterium. eLife 2: e01501.
77. Terra, R., Stanley-Wall, N.R., Cao, G., and Lazazzera, B.A. (2012) Identification of Bacillus subtilis SipW as a bifunctional signal peptidase that controls surface-adhered biofilm formation. J Bacteriol 194: 2781-2790.
78. Trejo, M., Douarche, C., Bailleux, V., Poulard, C., Mariot, S., Regeard, C., and Raspaud, E. (2013) Elasticity and wrinkled morphology of Bacillus subtilis pellicles. Proc Natl Acad Sci USA 110: 2011-2016.
79. Tucker, A.T., Bobay, B.G., Banse, A.V., Olson, A.L., Soderblom, E.J., Moseley, M.A., etal. (2014) A DNA mimic: the structure and mechanism of action for the anti-repressor protein AbbA. J Mol Biol 426: 1911-1924.
80. Veening, J.W., Kuipers, O.P., Brul, S., Hellingwerf, K.J., and Kort, R. (2006) Effects of phosphorelay perturbations on architecture, sporulation, and spore resistance in biofilms of Bacillus subtilis. J Bacteriol 188: 3099-3109.
81. Verhamme, D.T., Kiley, T.B., and Stanley-Wall, N.R. (2007) DegU co-ordinates multicellular behaviour exhibited by Bacillus subtilis. Mol Microbiol 65: 554-568.
82. Verhamme, D.T., Murray, E.J., and Stanley-Wall, N.R. (2009) DegU and Spo0A jointly control transcription of two loci required for complex colony development by Bacillus subtilis. J Bacteriol 191: 100-108.
83. Vlamakis, H., Aguilar, C., Losick, R., and Kolter, R. (2008) Control of cell fate by the formation of an architecturally complex bacterial community. Genes Dev 22: 945-953.
84. Vlamakis, H., Chai, Y., Beauregard, P., Losick, R., and Kolter, R. (2013) Sticking together: building a biofilm the Bacillus subtilis way. Nat Rev Microbiol 11: 157-168.
85. Wilking, J.N., Zaburdaev, V., De Volder, M., Losick, R., Brenner, M.P., and Weitz, D.A. (2013) Liquid transport facilitated by channels in Bacillus subtilis biofilms. Proc Natl Acad Sci USA 110: 848-852.
86. Winkelman, J.T., Blair, K.M., and Kearns, D.B. (2009) RemA (YlzA) and RemB (YaaB) regulate extracellular matrix operon expression and biofilm formation in Bacillus subtilis. J Bacteriol 191: 3981-3991.
87. Winkelman, J.T., Bree, A.C., Bate, A.R., Eichenberger, P., Gourse, R.L., and Kearns, D.B. (2013) RemA is a DNA-binding protein that activates biofilm matrix gene expression in Bacillus subtilis. Mol Microbiol 88: 984-997.
88. Zurdo, J., Guijarro, J.I., Jimenez, J.L., Saibil, H.R., and Dobson, C.M. (2001) Dependence on solution conditions of aggregation and amyloid formation by an SH3 domain. J Mol Biol 311: 325-340.