Cellulose as an architectural element in spatially structured escherichia coli biofilms

Journal of Bacteriology

Volumn 195, Issue 24, 2013, Pages 5540-5554

  Serra, Diego O ^a,b   Richter, Anja M ^a,b   Hengge, Regine ^a,b  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

^b HUMBOLDT UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELLULOSE;

ARTICLE; BACTERIUM COLONY; BIOFILM; CELL ADHESION; ELASTICITY; ELECTRON MICROSCOPY; ESCHERICHIA COLI; EXTRACELLULAR MATRIX; FLUORESCENCE MICROSCOPY; MICROBIAL MORPHOLOGY; NONHUMAN; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM;

BACTERIAL PROTEINS; BIOFILMS; CELLULOSE; ESCHERICHIA COLI K12; MICROSCOPY, ELECTRON, SCANNING; MICROSCOPY, FLUORESCENCE; POINT MUTATION;

EID: 84890155152     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00946-13     Document Type: Article

References (60)

1. Hall-Stoodley L, Costerton JW, Stoodley P. 2004. Bacterial biofilms: from the natural environment to infectious diseases. Nature Rev. Microbiol. 2:95-108.
2. Serra DO, Richter AM, Klauck G, Mika F, Hengge R. 2013. Microanatomy at cellular resolution and spatial order of physiological differentiation in a bacterial biofilm. mBio 4:e00103-13. doi:10.1128/mBio.00103-13.
3. Stewart PS, Franklin MJ. 2008. Physiological heterogeneity in biofilms. Nat. Rev. Microbiol. 6:199-210.
4. Aguilar C, Vlamakis H, Losick R, Kolter R. 2007. Thinking about Bacillus subtilis as a multicellular organism. Curr. Opin. Microbiol. 10:638-643.
5. Lim B, Beyhan S, Meir J, Yildiz FH. 2006. Cyclic-diGMP signal transduction systems in Vibrio cholerae: modulation of rugosity and biofilm formation. Mol. Microbiol. 60:331-348.
6. Mann EE, Wozniak DJ. 2012. Pseudomonas biofilm matrix composition and niche biology. FEMS Microbiol. Rev. 36:893-916.
7. Römling U. 2005. Characterization of the rdar morphotype, a multicellular behavior in Enterobacteriaceae. Cell. Mol. Life Sci. 62:1234-1246.
8. Jonas K, Tomenius H, Kader A, Normark S, Römling U, Belova LB, Melefors O. 2007. Roles of curli, cellulose and BapA in Salmonella biofilm morphology studied by atomic force microscopy. BMC Microbiol. 7:70. doi:10.1186/1471-2180-7-70.
9. Romero D, Aguilar C, Losick R, Kolter R. 2010. Amyloid fibres provide structural integrity to Bacillus subtilis biofilms. Proc. Natl. Acad. Sci. U.S.A. 107:2230-2234.
10. Vlamakis H, Chai Y, Beauregard P, Losick R, Kolter R. 2013. Sticking together: building a biofilm the Bacillus subtilis way. Nature Rev. Microbiol. 11:157-168.
11. Olsén A, Jonsson A, Normark S. 1989. Fibronectin binding mediated by a novel class of surface organelles on Escherichia coli. Nature 338:652-655.
12. Zogaj X, Nimtz M, Rohde M, Bokranz W, Römling U. 2001. The multicellular morphotypes of Salmonella typhimurium and Escherichia coli produce cellulose as the second component of the extracellular matrix. Mol. Microbiol. 39:1452-1463.
13. Barnhart MM, Chapman MR. 2006. Curli biogenesis and function. Annu. Rev. Microbiol. 60:131-147.
14. Chapman MR, Robinson LS, Pinkner JS, Roth R, Heuser J, Hammar M, Normark S, Hultgren SJ. 2002. Role of Escherichia coli curli operons in directing amyloid fiber formation. Science 295:851-855.
15. Morgan JLW, Strumillo J, Zimmer J. 2013. Crystallographic snapshot of cellulose synthesis and membrane translocation. Nature 493:181-186.
16. Whitney JC, Howell PL. 2013. Synthase-dependent exopolysaccharide secretion in Gram-negative bacteria. Trends Microbiol. 21:63-72.
17. Solano C, García B, Valle J, Berasain C, Ghigo J-M, Gamazo C, Lasa I. 2002. Genetic analysis of Salmonella enteritidis biofilm formation: critical role of cellulose. Mol. Microbiol. 43:793-808.
18. Bokranz W, Wang X, Tschape H, Römling U. 2005. Expression of cellulose and curli fimbriae by Escherichia coli isolated from the gastrointestinal tract. J. Med. Microbiol. 54:1171-1182.
19. Da Re S, Ghigo J-M. 2006. A CsgD-Independent pathway for cellulose production and biofilm formation in Escherichia coli. J. Bacteriol. 188:3073-3087.
20. Römling U, Sierralta WD, Eriksson K, Normark S. 1998. Multicellular and aggregative behavior of Salmonella typhimurium strains is controlled by mutations in the agfD promoter. Mol. Microbiol. 28:249-264.
21. Römling U, Rohde M, Olsén A, Normark S, Reinköster J. 2000. AgfD, the checkpoint of multicellular and aggregative behavior in Salmonella typhimurium regulates at least two independent pathways. Mol. Microbiol. 36:10-23.
22. Gualdi L, Tagliabue L, Bertagnoli S, Ieranò T, De Castro C, Landini P. 2008. Cellulose modulates biofilm formation by counteracting curlimediated colonization of solid surfaces in Escherichia coli. Microbiology 154:2017-2024.
23. Hengge R. 2009. Principles of cyclic-di-GMP signaling. Nat. Rev. Microbiol. 7:263-273.
24. Jenal U, Malone J. 2006. Mechanisms of cyclic-di-GMP signaling in bacteria. Annu. Rev. Genet. 40:385-407.
25. Römling U, Galperin MY, Gomelsky L. 2013. Cyclic-di-GMP: the first 25 years of a universal bacterial second messenger. Microb. Mol. Biol. Rev. 77:1-52.
26. Lindenberg S, Klauck G, Pesavento C, Klauck E, Hengge R. 2013. The EAL domain phosphodiesterase YciR acts as a trigger enzyme in a c-di- GMP signaling cascade in Escherichia coli biofilm control. EMBO J. 32:2001-2014.
27. Pesavento C, Becker G, Sommerfeldt N, Possling A, Tschowri N, Mehlis A, Hengge R. 2008. Inverse regulatory coordination of motility and curlimediated adhesion in Escherichia coli. Genes Dev. 22:2434-2446.
28. S network of Escherichia coli. Mol. Microbiol. 62:1014-1034.
29. García B, Latasa C, Solano C, García-del Portillo F, Gamazo C, Lasa I. 2004. Role of the GGDEF protein family in Salmonella cellulose biosynthesis and biofilm formation. Mol. Microbiol. 54:264-277.
30. Amikam D, Galperin MY. 2006. PilZ domain is part of the bacterial c-di-GMP binding protein. Bioinformatics 22:3-6.
31. Hayashi K, Morooka N, Yamamoto Y, Fujita K, Isono K, Choi S, Ohtsubo E, Baba T, Wanner BL, Mori H, Horiuchi T. 2006. Highly accurate genome sequences of Escherichia coli K-12 strains MG1655 and W3110. Mol. Syst. Biol. 2:2006.0007.
32. Datsenko KA, Wanner BL. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U.S.A. 97:6640-6645.
33. Miller JH. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
34. S) in Escherichia coli. RNA Biol. 8:913-921.
35. Simons RW, Houman F, Kleckner N. 1987. Improved single and multicopy lac-based cloning vectors for protein and operon fusions. Gene 53:85-96.
36. Powell BS, Court DL, Nakamura Y, Rivas MP, Turnbough CL, Jr. 1994 Rapid confirmation of single copy lambda prophage integration by PCR. Nucleic Acids Res. 22:5765-5766.
37. Uzzau S, Figueroa-Bossi N, Rubino S, Bossi L. 2001. Epitope tagging of chromosomal genes in Salmonella. Proc. Natl. Acad. Sci. U.S.A. 98: 15264-15269.
38. Weiss-Muszkat M, Shakh D, Zhou Y, Pinto R, Belausov E, Chapman MR, Sela S. 2010. Biofilm formation by and multicellular behavior of Escherichia coli O55:H7, an atypical enteropathogenic strain. Appl. Environ. Microbiol. 76:1545-1554.
39. Hengge R. 2011. The general stress response in Gram-negative bacteria, p 251-289. In Storz G, Hengge R (ed), Bacterial stress responses. ASM Press, Washington, DC.
40. Ferenci T. 2005. Maintaining a healthy SPANC balance through regulatory and mutational adaptation. Mol. Microbiol. 57:1-8.
41. DePas WH, Hufnagel DA, Lee JS, Blanco LP, Bernstein HC, Fisher ST, James GA, Stewart PS, Chapman MR. 2013. Iron induces bimodal population development by Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 110:2629-2634.
42. Klemm D, Kramer F, Moritz S, Lindström T, Ankerfors M, Gray D, Dorris A. 2011. Nanocelluloses: a new family of nature-based materials. Angew. Chem. Int. Ed. Engl. 50:5438-5466.
43. Siró I, Plackett D. 2010. Microfibrillated cellulose and new nanocomposite materials: a review. Cellulose 17:459-494.
44. Lim JY, May JM, Cegelski L. 2012. Dimethyl sulfoxide and ethanol elicit increased amyloid biogenesis and amyloid-integrated biofilm formation in Escherichia coli. Appl. Environ. Microbiol. 78:3369-3378.
45. Wu C, Lim JY, Fuller GG, Cegelski L. 2012. Quantitative analysis of amyloid-integrated biofilms formed by uropathogenic Escherichia coli at the air-liquid interface. Biophys. J. 103:464-471.
46. Asally M, Kittisopikul M, Rué P, Du Y, Hu Z, Cagatay T, Robinson AB, Lu H, Garcia-Ojalvo J, Süel GM. 2012. Localized cell death focuses mechanical forces during 3D patterning in a biofilm. Proc. Natl. Acad. Sci. U.S.A. 109:18891-18896.
47. Watnick P, Kolter R. 2000. Biofilm, city of microbes. J. Bacteriol. 182:2675-2679.
48. Larsen P, Nielsen JL, Dueholm MS, Wetzel R, Otzen D, Nielsen PH. 2007. Amyloid adhesins are abundant in natural biofilms. Environ. Microbiol. 9:3077-3090.
49. Blanco LP, Evans ML, Smith DR, Badtke MP, Chapman MR. 2012. Diversity, biogenesis and function of microbial amyloids. Trends Microbiol. 20:66-73.
50. Dietrich LE, Okegbe C, Price-Whelan A, Sakhtah H, Hunter RC, Newman DK. 2013. Bacterial community morphogenesis is intimately linked to the intracellular redox state. J. Bacteriol. 195:1371-1380.
51. Kolodkin-Gal I, Elsholz AK, Muth C, Girguis PR, Kolter R, Losick R. 2013. Respiration control of multicellularity in Bacillus subtilis by a complex of the cytochrome chain with a membrane-embedded histidine kinase. Genes Dev. 27:887-899.
52. Wilking JN, Zaburdaev V, De Volder M, Losick R, Brenner MP, Weitz DA. 2013. Liquid transport facilitated by channels in Bacillus subtilis biofilms. Proc. Natl. Acad. Sci. U.S.A. 110:848-852.
53. Brandl MT, Carter MQ, Parker CT, Chapman MR, Huynh S, Zhou Y. 2011. Salmonella biofilm formation on Aspergillus niger involves cellulosechitin interactions. PLoS One 6:e25553. doi:10.1371/journal.pone.0025553.
54. Laus MC, van Brussel AA, Kijne JW. 2005. Role of cellulose fibrils and exopolysaccharides of Rhizobium leguminosarum in attachment to and infection of Vicia sativa root hais. Mol. Plant-Microbe Interact. 18:533-538.
55. Tükel C, Nishimori JH, Wilson RP, Winter MG, Keestra AM, van Putten JP, Bäumler AJ. 2010. Toll-like receptors 1 and 2 cooperatively mediate immune responses to curli, a common amyloid from enterobacterial biofilms. Cell. Microbiol. 12:1495-1505.
56. Wang X, Rochon M, Lamprokostopoulou A, Lünsdorf H, Nimtz M, Römling U. 2006. Impact of biofilm matrix components on interaction of commensal Escherichia coli with the gastrointestinal cell line HT-29. Cell. Mol. Life Sci. 63:2352-2363.
57. Zorraquino V, García B, Latasa C, Echeverz M, Toledo-Arana A, Valle J, Lasa I, Solano C. 2013. Coordinated cyclic-di-GMP repression of Salmonella motility through YcgR and cellulose. J. Bacteriol. 195:417-428.
58. Römling U, Bian Z, Hammar M, Sierralta WD, Normark S. 1998. Curli fibers are highly conserved between Salmonella typhimurium and Escherichia coli with respect to operon structure and regulation. J. Bacteriol. 180:722-731.
59. Kader A, Simm R, Gerstel U, Morr M, Römling U. 2006. Hierarchical involvement of various GGDEF domain proteins in rdar morphotype development of Salmonella enterica serovar Typhimurium. Mol. Microbiol. 60:602-616.
60. Simm R, Lusch A, Kader A, Andersson M, Römling U. 2007. Role of EAL-containing proteins in multicellular behavior of Salmonella enterica serovar Typhimurium. J. Bacteriol. 189:3613-3623.