Sum of the parts: Composition and architecture of the bacterial extracellular matrix

Journal of Molecular Biology

Volumn 425, Issue 22, 2013, Pages 4286-4294

  McCrate, Oscar A ^a   Zhou, Xiaoxue ^a   Reichhardt, Courtney ^a   Cegelski, Lynette ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

biofilm; curli; extracellular matrix; functional amyloid; NMR

Indexed keywords

BACTERIAL PROTEIN; NITROGEN 15;

ARTICLE; BACTERIUM CULTURE; BIOFILM; CARBON NUCLEAR MAGNETIC RESONANCE; ESCHERICHIA COLI; EXTRACELLULAR MATRIX; ISOTOPE LABELING; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; SCANNING ELECTRON MICROSCOPY; TRANSMISSION ELECTRON MICROSCOPY; URINARY TRACT INFECTION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 84886720456     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2013.06.022     Document Type: Article

References (48)

1. J.W. Costerton, K.J. Cheng, G.G. Geesey, T.I. Ladd, J.C. Nickel, and M. Dasgupta Bacterial biofilms in nature and disease Annu Rev Microbiol 41 1987 435 464
2. H.C. Flemming Biofouling in water systems - cases, causes and countermeasures Appl Microbiol Biotechnol 59 2002 629 640
3. J.W. Costerton, Z. Lewandowski, D.E. Caldwell, D.R. Korber, and H.M. Lappinscott Microbial biofilms Annu Rev Microbiol 49 1995 711 745
4. L. Hall-Stoodley, J.W. Costerton, and P. Stoodley Bacterial biofilms: from the natural environment to infectious diseases Nat Rev Microbiol 2 2004 95 108
5. L. Cegelski, G.R. Marshall, G.R. Eldridge, and S.J. Hultgren The biology and future prospects of antivirulence therapies Nat Rev Microbiol 6 2008 17 27
6. R.M. Donlan, and J.W. Costerton Biofilms: survival mechanisms of clinically relevant microorganisms Clin Microbiol Rev 15 2002 167
7. J.L. del Pozo, and R. Patel The challenge of treating biofilm-associated bacterial infections Clin Pharmacol Ther 82 2007 204 209
8. H.C. Flemming, and J. Wingender The biofilm matrix Nat Rev Microbiol 8 2010 623 633
9. I.W. Sutherland Biofilm exopolysaccharides: a strong and sticky framework Microbiology 147 2001 3 9
10. X. Zogaj, M. Nimtz, M. Rohde, W. Bokranz, and U. Romling The multicellular morphotypes of Salmonella typhimurium and Escherichia coli produce cellulose as the second component of the extracellular matrix Mol Microbiol 39 2001 1452 1463
11. M.R. Chapman, L.S. Robinson, J.S. Pinkner, R. Roth, J. Heuser, and M. Hammar Role of Escherichia coli curli operons in directing amyloid fiber formation Science 295 2002 851 855
12. C.J. Alteri, J. Xicohtencatl-Cortes, S. Hess, G. Caballero-Olin, J.A. Giron, and R.L. Friedman Mycobacterium tuberculosis produces pili during human infection Proc Natl Acad Sci USA 104 2007 5145 5150
13. D.S. Capstick, A. Jomaa, C. Hanke, J. Ortega, and M.A. Elliot Dual amyloid domains promote differential functioning of the chaplin proteins during Streptomyces aerial morphogenesis Proc Natl Acad Sci USA 108 2011 9821 9826
14. M.S. Dueholm, S.V. Petersen, M. Sonderkaer, P. Larsen, G. Christiansen, and K.L. Hein Functional amyloid in Pseudomonas Mol Microbiol 77 2010 1009 1020
15. D. Romero, C. Aguilar, R. Losick, and R. Kolter Amyloid fibers provide structural integrity to Bacillus subtilis biofilms Proc Natl Acad Sci USA 107 2010 2230 2234
16. U. Romling, W.D. Sierralta, K. Eriksson, and S. Normark Multicellular and aggregative behaviour of Salmonella typhimurium strains is controlled by mutations in the agfD promoter Mol Microbiol 28 1998 249 264
17. P. Larsen, J.L. Nielsen, D. Otzenj, and P.H. Nielsen Amyloid-like adhesins produced by floc-forming and filamentous bacteria in activated sludge Appl Environ Microbiol 74 2008 1517 1526
18. P. Larsen, J.L. Nielsen, M.S. Dueholm, R. Wetzel, D. Otzen, and P.H. Nielsen Amyloid adhesins are abundant in natural biofilms Environ Microbiol 9 2007 3077 3090
19. K. Schwartz, A.K. Syed, R.E. Stephenson, A.H. Rickard, and B.R. Boles Functional amyloids composed of phenol soluble modulins stabilize Staphylococcus aureus biofilms PLoS Pathog 8 2012 e1002744
20. L. Cegelski, J.S. Pinkner, N.D. Hammer, C.K. Cusumano, C.S. Hung, and E. Chorell Small-molecule inhibitors target Escherichia coli amyloid biogenesis and biofilm formation Nat Chem Biol 5 2009 913 919
21. G.G. Anderson, K.W. Dodson, T.M. Hooton, and S.J. Hultgren Intracellular bacterial communities of uropathogenic Escherichia coli in urinary tract pathogenesis Trends Microbiol 12 2004 424 430
22. Y. Kai-Larsen, P. Luthje, M. Chromek, V. Peters, X. Wang, and A. Holm Uropathogenic Escherichia coli modulates immune responses and its curli fimbriae interact with the antimicrobial peptide LL-37 PLoS Pathog 6 2010 e1001010
23. C. Beloin, A. Roux, and J.M. Ghigo Escherichia coli biofilms Bacterial Biofilms 322 2008 249 289
24. M.A. Schembri, M. Givskov, and P. Klemm An attractive surface: gram-negative bacterial biofilms Sci STKE 2002 2002 re6
25. X. Zogaj, W. Bokranz, M. Nimtz, and U. Romling Production of cellulose and curli fimbriae by members of the family Enterobacteriaceae isolated from the human gastrointestinal tract Infect Immun 71 2003 4151 4158
26. S. Da Re, and J.M. Ghigo A CsgD-independent pathway for cellulose production and biofilm formation in Escherichia coli J Bacteriol 188 2006 3073 3087
27. J.Y. Lim, J.M. May, and L. Cegelski Dimethyl sulfoxide and ethanol elicit increased amyloid biogenesis and amyloid-integrated biofilm formation in Escherichia coli Appl Environ Microbiol 78 2012 3369 3378
28. O.A. McCrate, X. Zhou, and L. Cegelski Curcumin as an amyloid-indicator dye in E. coli Chem Commun 49 2013 4193 4195
29. O. Toke, and L. Cegelski REDOR applications in biology: an overview eMagRes 2007 John Wiley & Sons, Ltd Chichester, UK
30. X.X. Zhou, and L. Cegelski Nutrient-dependent structural changes in S. aureus peptidoglycan revealed by solid-state NMR spectroscopy Biochemistry 51 2012 8143 8153
31. L. Cegelski, and J. Schaefer Glycine metabolism in intact leaves by in vivo 13C and 15N labeling J Biol Chem 280 2005 39238 39245
32. K.J. Kramer, T.L. Hopkins, and J. Schaefer Analysis of intractable biological samples by solids NMR Nitrogen-containing macromolecules in the bio- and geosphere 707 1998 14 33
33. P.J. Wood, and R.G. Fulcher Interaction of some dyes with cereal beta-glucans Cereal Chem 55 1978 952 966
34. A.H. Delcour, Y. Zhou, D. Smith, D. Hufnagel, and M. Chapman Experimental manipulation of the microbial functional amyloid called curli Bacterial cell surfaces Vol. 966 2013 Humana Press New York 53 75
35. J.P. Lasserre, E. Beyne, S. Pyndiah, D. Lapaillerie, S. Claverol, and M. Bonneu A complexomic study of Escherichia coli using two-dimensional blue native/SDS polyacrylamide gel electrophoresis Electrophoresis 27 2006 3306 3321
36. D.L. Vanderhart, and R.H. Atalla Studies of microstructure in native celluloses using solid-state C-13 NMR Macromolecules 17 1984 1465 1472
37. A. Kai, P. Xu, F. Horii, and S.H. Hu CP/MAS C-13 NMR study on microbial cellulose fluorescent brightener complexes Polymer 35 1994 75 79
38. S. Maunu, T. Liitia, S. Kauliomaki, B. Hortling, and J. Sundquist C-13 CPMAS NMR investigations of cellulose polymorphs in different pulps Cellulose 7 2000 147 159
39. A. Varki Essentials of glycobiology 1999 Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY
40. T. Gullion, and J. Schaefer Rotational-echo double-resonance NMR J Magn Reson 81 1989 196 200
41. T.K. Lindhorst, S. Kotter, U. Krallmann-Wenzel, and S. Ehlers Trivalent alpha-d-mannoside clusters as inhibitors of type-1 fimbriae-mediated adhesion of Escherichia coli: structural variation and biotinylation J Chem Soc Perkin Trans 1 2001 823 831
42. C. Wu, J.Y. Lim, G.G. Fuller, and L. Cegelski Quantitative analysis of amyloid-integrated biofilms formed by uropathogenic Escherichia coli at the air-liquid interface Biophys J 103 2012 464 471
43. I.W. Sutherland The biofilm matrix - an immobilized but dynamic microbial environment Trends Microbiol 9 2001 222 227
44. Neidhard Fc, P.L. Bloch, and D.F. Smith Culture medium for Enterobacteria J Bacteriol 119 1974 736 747
45. F. Shewmaker, R.P. McGlinchey, K.R. Thurber, P. McPhie, F. Dyda, and R. Tycko The functional curli amyloid is not based on in-register parallel beta-sheet structure J Biol Chem 284 2009 25065 25076
46. J. Schaefer, and E.O. Stejskal C-13 nuclear magnetic-resonance of polymers spinning at magic angle J Am Chem Soc 98 1976 1031 1032
47. A.E. Bennett, C.M. Rienstra, M. Auger, K.V. Lakshmi, and R.G. Griffin Heteronuclear decoupling in rotating solids J Chem Phys 103 1995 6951 6958
48. D.O. Serra, A.M. Richter, G. Klauck, F. Mika, and R. Hengge Microanatomy at cellular resolution and spatial order of physiological differentiation in a bacterial biofilm Mbio 4 2 2013 10.1128/mBio.00103-13