Exopolymer Diversity and the Role of Levan in Bacillus subtilis Biofilms

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Dogsa, Iztok ^a   Brloznik, Mojca ^a   Stopar, David ^a   Mandic Mulec, Ines ^a  

^a UNIVERSITY OF LJUBLJANA   (Slovenia)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; BACTERIAL PROTEIN; EXOPOLYMER; LEVAN; POLYMER; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GROWTH; BIOFILM; CARBOHYDRATE ANALYSIS; CARBOHYDRATE SYNTHESIS; CULTURE MEDIUM; MICROBIAL DIVERSITY; PHENOTYPE; POLYMERIZATION; PROCESS DEVELOPMENT; STRAIN DIFFERENCE;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; BIOFILMS; BIOMASS; BIOPOLYMERS; CHROMATOGRAPHY, GEL; CULTURE MEDIA; FRUCTANS; GENE EXPRESSION REGULATION, BACTERIAL; NUCLEIC ACIDS; OPERON; PHENOTYPE; POLYSACCHARIDES, BACTERIAL; SUCROSE; TIME FACTORS;

BACILLUS SUBTILIS;

EID: 84876865624     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0062044     Document Type: Article

References (75)

1. Branda SS, Vik A, Friedman L, Kolter R, (2005) Biofilms: the matrix revisited. Trends Microbiol 13: 20-26.
2. 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.
3. Lasa I, (2006) Towards the identification of the common features of bacterial biofilm development. Int Microbiol 9: 21-28.
4. Sutherland IW, (2001) The biofilm matrix-an immobilized but dynamic microbial environment. Trends Microbiol 9: 222-227.
5. Vilain S, Pretorius JM, Theron J, Brözel VS, (2009) DNA as an adhesin: Bacillus cereus requires extracellular DNA to form biofilms. Appl Environ Microbiol 75: 2861-2868.
6. Whitchurch CB, Tolker-Nielsen T, Raga SPC, Mattick JS, (2002) Extracellular DNA required for bacterial biofilm formation. Science 295: 1487-1487.
7. Morita N, Takagi M. Murao S, (1979) A new gel-forming polysaccharide produced by Bacillus subtilis FT-3 its structure and its physical and chemical characteristics. Bull Uni Osaka Pref, Ser B 31: 27-41.
8. Morita N, Matsumoto S, Takagi M, (1982) Rheological properties of aqueous solutions of Bacillus subtilis FT-3 polysaccharide. Bull Uni Osaka Pref, Ser B 34: 57-66.
9. Chai Y, Beauregard PB, Vlamakis H, Losick R, Kolter R, (2012) Galactose Metabolism Plays a Crucial Role in Biofilm Formation by Bacillus subtilis. mBio 3: e00184-12.
10. Vijayabaskar P, Babinastarlin S, Shankar T, Sivakumar T, Anandapandian KTK, (2011) Quantification and characterization of exopolysaccharides from Bacillus subtilis (MTCC 121). Adv Biol Res (Rennes) 5: 71-76.
11. Branda SS, Gonzalez-Pastor JE, Ben-Yehuda S, Losick R, Kolter R, (2001) Fruiting body formation by Bacillus subtilis. Proc Natl Acad Sci U S A 98: 11621-11626.
12. Hamon MS, Lazazzera BA, (2001) The sporulation transcription factor Spo0A is required for biofilm development in Bacillus subtilis. Mol Microbiol 42: 1199-1209.
13. Kobayashi K, (2007) Bacillus subtilis pellicle formation proceeds through genetically defined morphological changes. J Bacteriol 189: 4920-4931.
14. Marvasi M, Visscher PT, Martinez LC, (2010) Exopolymeric substances (EPS) from Bacillus subtilis: polymers and genes encoding their synthesis. FEMS Microbiol Lett 313: 1-9.
15. Branda SS, Gonzalez-Pastor JE, Dervyn E, Ehrlich SD, Losick R, et al. (2004) Genes involved in formation of structured multicellular communities by Bacillus subtilis. J Bacteriol 186: 3970-3979.
16. Driks A, (2011) Tapping into the biofilm: insights into assembly and disassembly of a novel amyloid fibres in Bacillus subtilis. Mol Microbiol 80: 1133-1136.
17. Lopez D, Fischbach MA, Chu F, Losick R, Kolter R, (2009) Structurally diverse natural products that cause potassium leakage trigger multicellularity in Bacillus subtilis. Proc Natl Acad Sci U S A 106: 280-285.
18. Ostrowski A, Melhert A, Prescott A, Kiley TB, Stanley-Wall NR, (2011) YuaB functions synergistically with the exopolysaccharide and TasA amyloid fibers to allow biofilm formation by Bacillus subtilis. J Bacteriol 193: 4821-1831.
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. Chai Y, Chu F, Kolter R, Losick R, (2008) Bistability and biofilm formation in Bacillus subtilis. Mol Microbiol 67: 254-63.
21. Stover A, Driks A, (1999) Secretion, localization, and antibacterial activity of TasA, a Bacillus subtilis spore-associated protein. J Bacteriol 181: 1664-1672.
22. Romero D, Aguilar C, Losick R, Kolter R, (2009) Amyloid fibers provide structural integrity to Bacillus subtilis biofilms. Proc Natl Acad Sci U S A 107: 2230-2234.
23. Romero D, Vlamakis H, Losick R, Kolter R, (2011) An accessory protein required for anchoring and assembly of amyloid fibres in B. subtilis biofilms. Mol Microbiol 80: 1155-1168.
24. Stanley NR, Lazazzera BA, (2005) Defining the genetic differences between wild and domestic strains of Bacillus subtilis that affect poly- γ-DL-glutamic acid production and biofilm formation. Mol Microbiol 57: 1143-1158.
25. Morikawa M, Kagihiro S, Haruki M, Takano K, Branda S, et al. (2006) Biofilm formation by a Bacillus subtilis strain that produces γ-polyglutamate. Microbiology 152: 2801-2807.
26. Kobayashi K, Iwano M, (2012) BslA (YuaB) forms a hydrophobic layer on the surface of Bacillus subtilis biofilms. Mol Microbiol 85: 51-66.
27. Kovács ÁT, van Gestel J, Kuipers OP, (2012) The protective layer of biofilm: a repellent function for a new class of amphiphilic proteins. Mol Microbiol (2012) 85: 8-11.
28. Shih IL, Yu YT, Shieh CJ, Hsieh CY, (2005) Selective production and characterization of levan by Bacillus subtilis (Natto) Takahashi. J Agric Food Chem 53: 8211-8215.
29. Shih IL, Chen LD, Wu JY, (2010) Levan production using Bacillus subtilis natto cells immobilized on alginate. Carbohydr Polym 82: 111-117.
30. Lepesant JA, Kunst F, Lepesant-Kejzlarova J, Dedonder R, (1972) Chromosomal location of mutations affecting sucrose metabolism in Bacillus subtilis Marburg. Mol Gen Genet 118: 135-160.
31. Lepesant JA, Kunst F, Pascal M, Lepesant-Kejzlarova J, Steinmetz M, et al. (1976) Specific and pleiotropic regulatory mechanisms in the sucrose system of Bacillus subtilis 168. In: Schlessinger D, editor. Microbiology. Washington, D.C.: American Society for Microbiology. pp. 58-69.
32. Shimotsu H, Henner DJ, (1986) Modulation of Bacillus subtilis levansucrase gene expression by sucrose and regulation of the steady-state mRNA level by sacU and sacQ genes. J Bacteriol 168: 380-388.
33. Kang SA, Jang KH, Seo JW, Kim KH, Kim YH, et al. (2009) Levan: applications and perspectives. In: Rehm BHA, editor. Production of biopolymers and polymer precursors: applications and perspectives. New Zealand: Caister Academic Press. p. 145.
34. Meng G, Fütterer K, (2003) Structural framework of fructosyl transfer in Bacillus subtilis levansucrase. Nat Struct Mol Biol 10: 935-941.
35. Pereira Y, Petit-Glatron MF, Chambert R, (2001) yveB, encoding endolevanase LevB, is part of the sacB-yveB-yveA levansucrase tricistronic operon in Bacillus subtilis. Microbiology 147: 3413-3419.
36. Débarbouillé M, Martin V, Arnaud M, Klier A, Rapoport G, (1991) Positive and negative regulation controlling expression of the sac genes in Bacillus subtilis. Res Microbiol 142: 757-764.
37. Bais HP, Fall R, Vivanco JM, (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.
38. Chen Y, Cao S, Chai Y, Clardy J, Kolter R, et al. (2012) A Bacillus subtilis sensor kinase involved in triggering biofilm formation on the roots of tomato plants. Mol Microbiol 85: 418-430.
39. Chen Y, Yan F, Chai Y, Liu H, Kolter R, et al. (2012) Biocontrol of tomato wilt disease by Bacillus subtilis isolates from natural environments depends on conserved genes mediating biofilm formation. Environ Microbiol: in press doi: 10.1111/j.1462-2920.2012.02860.x. [Epub ahead of print].
40. Hess D, Heinrich D, Kemner J, Jekel S (1985) Secretion and cleavage of sucrose by wheat. A system of chemotactic attraction and nitrogenase induction in Azospirillum lipoferum. In: Klingmuller W, editor. Azospirillum III: Genetics, Physiology, Ecology. Berlin: Springer-Verlag. pp. 147-162.
41. Shida T, Mukaijo K, Ishikawa S, Yamamoto H, Sekiguchi J, (2002) Production of long-chain levan by a sacC insertional mutant from Bacillus subtilis 327UH. Biosci Biotechnol Biochem 66: 1555-1558.
42. Conn HJ, (1930) The identity of Bacillus subtilis. J Infect Dis 44: 341-350.
43. Hageman JH, Shankweiler GW, Wall PR, Franich K, McCowan GW, et al. (1984) Single, chemically defined sporulation medium for Bacillus subtilis: growth, sporulation, and extracellular protease production. J Bacteriol 160: 438-441.
44. Bakke R, Olsson PQ, (1986) Biofilm thickness measurements by light microscopy. J Microbiol Methods 5: 93-98.
45. White GW, (1970) Improving the accuracy of vertical measurements under the microscope. Microscope 18: 51-59.
46. Adav SS, Lee DJ, (2008) Extraction of extracellular polymeric substances from aerobic granule with compact interior structure. J Hazard Mater 154: 1120-1126.
47. Liu H, Fang HHP, (2002) Extraction of extracellular polymeric substances (EPS) of sludges. J Biotechnol 95: 249-256.
48. Pan X, Liu J, Zhang D, Chen X, Li L, et al. (2010) A comparison of five extraction methods for extracellular polymeric substances (EPS) from biofilm by using three-dimensional excitation-emission matrix (3DEEM) fluorescence spectroscopy. Water SA 36: 111-116.
49. Seviour T, Lambert LK, Pijuan M, Yuan Z, (2010) Structural determination of a key exopolysaccharide in mixed cultureaerobic sludge granules using NMR spectroscopy. Environ Sci Technol 44: 8964-8970.
50. Seviour T, Yuan Z, Donose BC, van Loosdrecht MCM, Lin Y, (2012) Aerobic sludge granulation: A tale of two polysaccharides? Water res 46: 4803-4813.
51. Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F, (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28: 350-356.
52. Jones RW, Erlander SR, (1967) Interaction between wheat proteins and dextrans. Cereal Chem 44: 447-456.
53. Laue H, Schenk A, Li H, Lambertsen L, Neu TR, et al. (2006) Contribution of alginate and levan production to biofilm formation by Pseudomonas syringae. Microbiology 152: 2909-2918.
54. Oliveira R, Marques F, Azeredo J, (1999) Purification of polysaccharides from a biofilm matrix by selective precipitation of proteins. Biotechnol Tech 13: 391-393.
55. Purama RK, Goswami P, Khan AT, Goyal A, (2008) Structural analysis and properties of dextran produced by Leuconostoc mesenteroides NRRL B-640. Carbohydr Polym 76: 30-35.
56. Cuesta G, Suarez N, Bessio MI, Ferreira F, Massaldi H, (2003) Quantitative determination of pneumococcal capsular polysaccharide serotype 14 using a modification of phenol-sulfuric acid method. J Microbiol Methods 52: 69-73.
57. Bradford MM, (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
58. Dogsa I, Kriechbaum M, Stopar D, Laggner P, (2005) Structure of bacterial extracellular polymeric substances at different pH values as determined by SAXS. Biophys J 89: 2711-2720.
59. Stoscheck CM, (1990) Quantitation of protein. Methods Enzymol 182: 50-68.
60. Glasel JA, (1995) Validity of nucleic acid purities monitored by A260/A280 absorbance ratios. Biotechniques 18: 62-63.
61. Muro AC, Rodriguez E, Abate CM, Siiqeriz F, (1999) Identification in TLC of fructose and fructosyl derivatives in levan and sugar mixtures with resorcinol and thiourea. Folia Microbiol 44: 647-649.
62. Rhee SK, Song KB, Kim CH, Park BS, Jang EK, et al. (2005) Levan. In: Steinbüchel A, editor. Biopolymers Online. Weinheim: Willey-WCH Verlag.
63. Model MA, Burkhardt JK, (2001) A standard for calibration and shading correction of a fluorescence microscope. Cytometry 44: 309-316.
64. Omoike A, Chorover J, (2004) Spectroscopic study of extracellular polymeric substances from Bacillus subtilis: Aqueous chemistry and adsorption effects. Biomacromolecules 5: 1219-1230.
65. Burne RA, Chen YY, Wexler DL, Kuramitsu H, Bowen WH, (1996) Cariogenicity of Streptococcus mutans strains with defects in fructan metabolism assessed in a program-fed specific-pathogen-free rat model. J Dent Res 75: 1572-1577.
66. Manandhar S, Vidhate S, D′Souza N, (2009) Water soluble levan polysaccharide biopolymer electrospun fibers. Carbohydr Polym 78: 794-798.
67. Arvidson SA, Rinehart BT, Gadala-Maria F, (2006) Concentration regimes of solutions of levan polysaccharide from Bacillus sp. Carbohydr Polym 65: 144-149.
68. So LL, Goldstein IJ, (1969) Protein-carbohydrate interaction. Carbohyd Res 10: 231-244.
69. Sutherland IW, (2001) Biofilm exopolysaccharides: a strong and sticky framework. Microbiology 147: 3-9.
70. Flemming HC, Wingender J, (2010) The biofilm matrix. Nat Rev Microbiol 8: 623-633.
71. Marschner H (1995) Mineral nutrition of higher plants. 2nd ed. London: Academic Press.889 p.
72. Mandić-Mulec I, Prosser JI (2011) Diversity of endospore-forming bacteria in soil: characterization and driving mechanisms. In: Logan NA, De Vos P, editors. Endospore-forming soil bacteria, (Soil biology, 27). 1st ed. Berlin: Springer-Verlag. pp. 31-59.
73. Štefanič P, Mandić-Mulec I, (2009) Social interactions and distribution of Bacillus subtilis pherotypes at microscale. J Bacteriol 191: 1756-1764.
74. Štefanič P, Decorsi F, Viti C, Petito J, Cohan F, et al. (2012) The quorum sensing diversity within and between ecotypes of Bacillus subtilis. Environ microbiol 14: 1378-1389.
75. Martin-Verstraete I, Stülke J, Klier A, Rapoport G, (1995) Two different mechanisms mediate catabolite repression of the Bacillus subtilis levanase operon. J Bacteriol 177: 6919-6927.