Stress responses go three dimensional - The spatial order of physiological differentiation in bacterial macrocolony biofilms

Environmental Microbiology

Volumn 16, Issue 6, 2014, Pages 1455-1471

  Serra, Diego O ^a   Hengge, Regine ^a  

^a HUMBOLDT UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFECTIVE AGENT; SIGMA FACTOR;

ADAPTATION; BIOFILM; CYTOLOGY; ESCHERICHIA COLI; EXTRACELLULAR MATRIX; HUMAN; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; SECOND MESSENGER;

ADAPTATION, PHYSIOLOGICAL; ANTI-BACTERIAL AGENTS; BIOFILMS; ESCHERICHIA COLI; EXTRACELLULAR MATRIX; HUMANS; METABOLIC NETWORKS AND PATHWAYS; SECOND MESSENGER SYSTEMS; SIGMA FACTOR; STRESS, PHYSIOLOGICAL;

EID: 84925273188     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12483     Document Type: Short Survey

References (146)

1. Adler, J., and Templeton, B. (1967) The effect of environmental conditions on the motility of Escherichia coli. J Gen Microbiol 46: 175-184.
2. Aguilar, C., Vlamakis, H., Losick, R., and Kolter, R. (2007) Thinking about Bacillus subtilis as a multicellular organism. Curr Opin Microbiol 10: 638-643.
3. Amsler, C.D., Cho, M., and Matsumura, P. (1993) Multiple factors underlying the maximum motility of Escherichia coli as cultures enter post-exponential growth. J Bacteriol 175: 6238-6244.
4. An, D., and Parsek, M.R. (2007) The promise and peril of transcriptional profiling in biofilm communities. Curr Opin Microbiol 10: 292-296.
5. Anderl, J.N., Zahller, J., Roe, F., and Stewart, P.S. (2003) Role of nutrient limitation and stationary-phase existence in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin. Antimicrob Agents Chemother 47: 1251- 1256.
6. Banta, A.B., Chumanov, R.S., Yuan, A.H., Lin, H., Campbell, E.A., Burgess, R.R., and Gourse, R.L. (2013) Key features of sigmaS required for specific recognition by Crl, a transcription factor promoting assembly of RNA polymerase holoenzyme. Proc Natl Acad Sci USA 110: 15955- 15960.
7. Barembruch, C., and Hengge, R. (2007) Cellular levels and activity of the flagellar sigma factor FliA of Escherichia coli are controlled by FlgM-modulated proteolysis. Mol Microbiol 65: 76-89.
8. Beech, I.B., and Sunner, J. (2004) Biocorrosion: towards understanding interactions between biofilms and metals. Curr Opin Biotechnol 15: 181-186.
9. Beloin, C., and Ghigo, J.M. (2005) Finding gene-expression patterns in bacterial biofilms. Trends Microbiol 13: 16-19.
10. Beloin, C., Valle, J., Latour-Lambert, P., Faure, P., Kzreminski, M., Balestrino, D., et al. (2004) Global impact of mature biofilm lifestyle on Escherichia coli K-12 gene expression. Mol Microbiol 51: 659-674.
11. Beyhan, S., Bilecen, K., Salama, S.R., Casper-Lindley, C., and Yildiz, F.H. (2007) Regulation of rugosity and biofilm formation in Vibrio cholerae: comparison of VpsT and VpsR regulons and epistasis analysis of vpsT, vpsR, and hapR. J Bacteriol 189: 388-402.
12. Bjarnsholt, T., Alhede, M., Alhede, M., Eickhardt-Sorensen, S.R., Moser, C., Kuhl, M., et al. (2013) The in vivo biofilm. Trends Microbiol 21: 466-474.
13. Boehm, A., Kaiser, M., Li, H., Spangler, C., Kasper, C.A., Ackermann, M., et al. (2010) Second messenger-mediated adjustment of bacterial swimming velocity. Cell 141: 107- 116.
14. Bokranz, W., Wang, X., Tschape, H., and Römling, U. (2005) Expression of cellulose and curli fimbriae by Escherichia coli isolated from the gastrointestinal tract. J Med Microbiol 54: 1171-1182.
15. Botsford, J.L., and Harman, J.G. (1992) Cyclic AMP in prokaryotes. Microbiol Rev 56: 100-122.
16. Bougdour, A., Lelong, C., and Geiselmann, J. (2004) Crl, a low temperature-induced protein in Escherichia coli that binds directly to the stationary phase sigma subunit of RNA polymerase. J Biol Chem 279: 19540-19550.
17. Boyd, C.D., and O'Toole, G.A. (2012) Second messenger regulation of biofilm formation: breakthroughs in understanding c-di-GMP effector systems. Annu Rev Cell Dev Biol 28: 439-462.
18. 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.
19. Brombacher, E., Dorel, C., Zehnder, A.J., and Landini, P. (2003) The curli biosynthesis regulator CsgD co-ordinates the expression of both positive and negative determinants for biofilm formation in Escherichia coli. Microbiology 149: 2847-2857.
20. Brombacher, E., Baratto, A., Dorel, C., and Landini, P. (2006) Gene expression regulation by the Curli activator CsgD protein: modulation of cellulose biosynthesis and control of negative determinants for microbial adhesion. J Bacteriol 188: 2027-2037.
21. Brown, P.K., Dozois, C.M., Nickerson, C.A., Zuppardo, A., Terlonge, J., and Curtiss, R., 3rd (2001) MlrA, a novel regulator of curli (AgF) and extracellular matrix synthesis by Escherichia coli and Salmonella enterica serovar Typhimurium. Mol Microbiol 41: 349-363.
22. Chai, Y., Chu, F., Kolter, R., and Losick, R. (2008) Bistability and biofilm formation in Bacillus subtilis. Mol Microbiol 67: 254-263.
23. Chevance, F.F., and Hughes, K.T. (2008) Coordinating assembly of a bacterial macromolecular machine. Nat Rev Microbiol 6: 455-465.
24. Chilcott, G.S., and Hughes, K.T. (2000) Coupling of flagellar gene expression to flagellar assembly in Salmonella enterica serovar typhimurium and Escherichia coli. Microbiol Mol Biol Rev 64: 694-708.
25. Christensen, B.B., Sternberg, C., Andersen, J.B., Palmer, R.J., Jr, Nielsen, A.T., Givskov, M., and Molin, S. (1999) Molecular tools for study of biofilm physiology. Methods Enzymol 310: 20-42.
26. Cohn, F. (1876) Untersuchungen über Bakterien IV: Beiträge zur Biologie der Bacillen. Beitr Biol Pflanzen 7: 249-276.
27. Colvin, K.M., Irie, Y., Tart, C.S., Urbano, R., Whitney, J.C., Ryder, C., et al. (2012) The Pel and Psl polysaccharides provide Pseudomonas aeruginosa structural redundancy within the biofilm matrix. Environ Microbiol 14: 1913- 1928.
28. Costerton, J.W., Cheng, K.J., Geesey, G.G., Ladd, T.I., Nickel, J.C., Dasgupta, M., and Marrie, T.J. (1987) Bacterial biofilms in nature and disease. Annu Rev Microbiol 41: 435-464.
29. Costerton, J.W., Stewart, P.S., and Greenberg, E.P. (1999) Bacterial biofilms: a common cause of persistent infections. Science 284: 1318-1322.
30. Da Re, S., and Ghigo, J.M. (2006) A CsgD-independent pathway for cellulose production and biofilm formation in Escherichia coli. J Bacteriol 188: 3073-3087.
31. Das, T., Sehar, S., and Manefield, M. (2013) The roles of extracellular DNA in the structural integrity of extracellular polymeric substance and bacterial biofilm development. Environ Microbiol Rep 5: 778-786.
32. DePas, W.H., Hufnagel, D.A., Lee, J.S., Blanco, L.P., Bernstein, H.C., Fisher, S.T., et al. (2013) Iron induces bimodal population development by Escherichia coli. Proc Natl Acad Sci USA 110: 2629-2634.
33. Dietrich, L.E., Okegbe, C., Price-Whelan, A., Sakhtah, H., Hunter, R.C., and Newman, D.K. (2013) Bacterial community morphogenesis is intimately linked to the intracellular redox state. J Bacteriol 195: 1371-1380.
34. Domka, J., Lee, J., Bansal, T., and Wood, T.K. (2007) Temporal gene-expression in Escherichia coli K-12 biofilms. Environ Microbiol 9: 332-346.
35. Dubnau, D., and Losick, R. (2006) Bistability in bacteria. Mol Microbiol 61: 564-572.
36. Evans, M.L., and Chapman, M.R. (2013) Curli biogenesis: order out of disorder. Biochim Biophys Acta. Available from URL: http://dx.doi.org/10.1016/j.bbamcr.2013.09.010.
37. Fang, X., and Gomelsky, M. (2010) A post-translational, c-di-GMP-dependent mechanism regulating flagellar motility. Mol Microbiol 76: 1295-1305.
38. Ferenci, T. (2001) Hungry bacteria - definition and properties of a nutritional state. Environ Microbiol 3: 605-611.
39. Ferenci, T. (2005) Maintaining a healthy SPANC balance through regulatory and mutational adaptation. Mol Microbiol 57: 1-8.
40. Ferenci, T. (2008) The spread of a beneficial mutation in experimental bacterial populations: the influence of the environment and genotype on the fixation of rpoS mutations. Heredity (Edinb) 100: 446-452.
41. Finkel, S.E. (2006) Long-term survival during stationary phase: evolution and the GASP phenotype. Nat Rev Microbiol 4: 113-120.
42. Flemming, H.C., and Wingender, J. (2010) The biofilm matrix. Nat Rev Microbiol 8: 623-633.
43. Fong, J.C., and Yildiz, F.H. (2007) The rbmBCDEF gene cluster modulates development of rugose colony morphology and biofilm formation in Vibrio cholerae. J Bacteriol 189: 2319-2330.
44. Fong, J.C., Karplus, K., Schoolnik, G.K., and Yildiz, F.H. (2006) Identification and characterization of RbmA, a novel protein required for the development of rugose colony morphology and biofilm structure in Vibrio cholerae. J Bacteriol 188: 1049-1059.
45. Friedman, L., and Kolter, R. (2004) Genes involved in matrix formation in Pseudomonas aeruginosa PA14 biofilms. Mol Microbiol 51: 675-690.
46. Frye, J., Karlinsey, J.E., Felise, H.R., Marzolf, B., Dowidar, N., McClelland, M., and Hughes, K.T. (2006) Identification of new flagellar genes of Salmonella enterica serovar Typhimurium. J Bacteriol 188: 2233-2243.
47. Gerstel, U., and Römling, U. (2003) The csgD promoter, a control unit for biofilm formation in Salmonella typhimurium. Res Microbiol 154: 659-667.
48. Girgis, H.S., Liu, Y., Ryu, W.S., and Tavazoie, S. (2007) A comprehensive genetic characterization of bacterial motility. PLoS Genet 3: 1644-1660.
49. Gloag, E.S., Turnbull, L., Huang, A., Vallotton, P., Wang, H., Nolan, L.M., et al. (2013) Self-organization of bacterial biofilms is facilitated by extracellular DNA. Proc Natl Acad Sci USA 110: 11541-11546.
50. Gophna, U., Barlev, M., Seijffers, R., Oelschlager, T.A., Hacker, J., and Ron, E.Z. (2001) Curli fibers mediate internalization of Escherichia coli by eukaryotic cells. Infect Immun 69: 2659-2665.
51. Gorbushina, A.A., and Broughton, W.J. (2009) Microbiology of the atmosphere-rock interface: how biological interactions and physical stresses modulate a sophisticated microbial ecosystem. Annu Rev Microbiol 63: 431-450.
52. Grainger, D.C., Hurd, D., Harrison, M., Holdstock, J., and Busby, S.J. (2005) Studies of the distribution of Escherichia coli cAMP-receptor protein and RNA polymerase along the E. coli chromosome. Proc Natl Acad Sci USA 102: 17693-17698.
53. Grigorova, I.L., Phleger, N.J., Mutalik, V.K., and Gross, C.A. (2006) Insights into transcriptional regulation and sigma competition from an equilibrium model of RNA polymerase binding to DNA. Proc Natl Acad Sci USA 103: 5332-5337.
54. Hall-Stoodley, L., and Stoodley, P. (2005) Biofilm formation and dispersal and the transmission of human pathogens. Trends Microbiol 13: 7-10.
55. Haussler, S., and Fuqua, C. (2013) Biofilms 2012: new discoveries and significant wrinkles in a dynamic field. J Bacteriol 195: 2947-2958.
56. Hengge, R. (2009a) Proteolysis of sigmaS (RpoS) and the general stress response in Escherichia coli. Res Microbiol 160: 667-676.
57. Hengge, R. (2009b) Principles of c-di-GMP signalling in bacteria. Nat Rev Microbiol 7: 263-273.
58. Hengge, R. (2010) Role of c-di-GMP in the regulatory networks of Escherichia coli. In The Second Messenger Cyclic-di-GMP. Wolfe, A.J., and Visick, K.L. (eds). Washington, DC: ASM Press, pp. 230-252.
59. Hengge, R. (2011) The general stress response in gramnegative bacteria. In Bacterial Stress Responses. Storz, G., and Hengge, R. (eds). Washington, DC: ASM press, pp. 251-289.
60. Hentzer, M., Eberl, L., and Givskov, M. (2005) Transcriptome analysis of Pseudomonas aeruginosa biofilm development: anaerobic respiration and iron limitation. Biofilms 2: 37-61.
61. Hoiby, N., Bjarnsholt, T., Givskov, M., Molin, S., and Ciofu, O. (2010) Antibiotic resistance of bacterial biofilms. Int J Antimicrob Agents 35: 322-332.
62. Hooshangi, S., Thiberge, S., and Weiss, R. (2005) Ultrasensitivity and noise propagation in a synthetic transcriptional cascade. Proc Natl Acad Sci USA 102: 3581- 3586.
63. Ishihama, A. (2000) Functional modulation of Escherichia coli RNA polymerase. Annu Rev Microbiol 54: 499-518.
64. Jenal, U., and Malone, J. (2006) Mechanisms of cyclic-di-GMP signaling in bacteria. Annu Rev Genet 40: 385-407.
65. Jishage, M., and Ishihama, A. (1998) A stationary phase protein in Escherichia coli with binding activity to the major sigma subunit of RNA polymerase. Proc Natl Acad Sci USA 95: 4953-4958.
66. Jishage, M., and Ishihama, A. (1999) Transcriptional organization and in vivo role of the Escherichia coli rsd gene, encoding the regulator of RNA polymerase sigma D. J Bacteriol 181: 3768-3776.
67. Jishage, M., Kvint, K., Shingler, V., and Nystrom, T. (2002) Regulation of sigma factor competition by the alarmone ppGpp. Genes Dev 16: 1260-1270.
68. Jørgensen, M.G., Nielsen, J.S., Boysen, A., Franch, T., Moller-Jensen, J., and Valentin-Hansen, P. (2012) Small regulatory RNAs control the multi-cellular adhesive lifestyle of Escherichia coli. Mol Microbiol 84: 36-50.
69. Jubelin, G., Vianney, A., Beloin, C., Ghigo, J.M., Lazzaroni, J.C., Lejeune, P., and Dorel, C. (2005) CpxR/OmpR interplay regulates curli gene expression in response to osmolarity in Escherichia coli. J Bacteriol 187: 2038-2049.
70. Klauck, E., and Hengge, R. (2011) σS-controlling networks in Escherichia coli. In Bacterial Regulatory Networks. Filloux, A.A.M. (ed.). Norfolk, UK: Caister Academic Press, pp. 1-26.
71. Ko, M., and Park, C. (2000) Two novel flagellar components and H-NS are involved in the motor function of Escherichia coli. J Mol Biol 303: 371-382.
72. Kolodkin-Gal, I., Elsholz, A.K., Muth, C., Girguis, P.R., Kolter, R., and 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.
73. Krasteva, P.V., Giglio, K.M., and Sondermann, H. (2012) Sensing the messenger: the diverse ways that bacteria signal through c-di-GMP. Protein Sci 21: 929-948.
74. Kroos, L. (2007) The Bacillus and Myxococcus developmental networks and their transcriptional regulators. Annu Rev Genet 41: 13-39.
75. Lange, R., and Hengge-Aronis, R. (1991a) Identification of a central regulator of stationary-phase gene expression in Escherichia coli. Mol Microbiol 5: 49-59.
76. Lange, R., and Hengge-Aronis, R. (1991b) Growth phaseregulated expression of bolA and morphology of stationaryphase Escherichia coli cells are controlled by the novel sigma factor sigma S. J Bacteriol 173: 4474-4481.
77. Lange, R., Fischer, D., and Hengge-Aronis, R. (1995) Identification of transcriptional start sites and the role of ppGpp in the expression of rpoS, the structural gene for the sigma S subunit of RNA polymerase in Escherichia coli. J Bacteriol 177: 4676-4680.
78. Larsen, P., Nielsen, J.L., Dueholm, M.S., Wetzel, R., Otzen, D., and Nielsen, P.H. (2007) Amyloid adhesins are abundant in natural biofilms. Environ Microbiol 9: 3077- 3090.
79. Lemke, J.J., Durfee, T., and Gourse, R.L. (2009) DksA and ppGpp directly regulate transcription of the Escherichia coli flagellar cascade. Mol Microbiol 74: 1368-1379.
80. Lindenberg, S., Klauck, G., Pesavento, C., Klauck, E., and Hengge, R. (2013) The EAL domain protein YciR acts as a trigger enzyme in a c-di-GMP signalling cascade in E. coli biofilm control. EMBO J 32: 2001-2014.
81. Lipshtat, A., Loinger, A., Balaban, N.Q., and Biham, O. (2006) Genetic toggle switch without cooperative binding. Phys Rev Lett 96: 188101.
82. Liu, M., Durfee, T., Cabrera, J.E., Zhao, K., Jin, D.J., and Blattner, F.R. (2005) Global transcriptional programs reveal a carbon source foraging strategy by Escherichia coli. J Biol Chem 280: 15921-15927.
83. Liu, X., and Matsumura, P. (1994) The FlhD/FlhC complex, a transcriptional activator of the Escherichia coli flagellar class II operons. J Bacteriol 176: 7345-7351.
84. Lopez, D., Vlamakis, H., Losick, R., and Kolter, R. (2009a) Paracrine signaling in a bacterium. Genes Dev 23: 1631- 1638.
85. Lopez, D., Vlamakis, H., Losick, R., and Kolter, R. (2009b) Cannibalism enhances biofilm development in Bacillus subtilis. Mol Microbiol 74: 609-618.
86. Malpica, R., Franco, B., Rodriguez, C., Kwon, O., and Georgellis, D. (2004) Identification of a quinone-sensitive redox switch in the ArcB sensor kinase. Proc Natl Acad Sci USA 101: 13318-13323.
87. Mann, E.E., and Wozniak, D.J. (2012) Pseudomonas biofilm matrix composition and niche biology. FEMS Microbiol Rev 36: 893-916.
88. Matz, C., McDougald, D., Moreno, A.M., Yung, P.Y., Yildiz, F.H., and Kjelleberg, S. (2005) Biofilm formation and phenotypic variation enhance predation-driven persistence of Vibrio cholerae. Proc Natl Acad Sci USA 102: 16819- 16824.
89. Mika, F., and Hengge, R. (2005) A two-component phosphotransfer network involving ArcB, ArcA, and RssB coordinates synthesis and proteolysis of sigmaS (RpoS) in E. coli. Genes Dev 19: 2770-2781.
90. Mika, F., and Hengge, R. (2013) Small regulatory RNAs in the control of motility and biofilm formation in E. coli and Salmonella. Int J Mol Sci 14: 4560-4579.
91. Mika, F., Busse, S., Possling, A., Berkholz, J., Tschowri, N., Sommerfeldt, N., et al. (2012) Targeting of csgD by the small regulatory RNA RprA links stationary phase, biofilm formation and cell envelope stress in Escherichia coli. Mol Microbiol 84: 51-65.
92. Moller, S., Pedersen, A.R., Poulsen, L.K., Arvin, E., and Molin, S. (1996) Activity and three-dimensional distribution of toluene-degrading Pseudomonas putida in a multispecies biofilm assessed by quantitative in situ hybridization and scanning confocal laser microscopy. Appl Environ Microbiol 62: 4632-4640.
93. Nguyen, D., Joshi-Datar, A., Lepine, F., Bauerle, E., Olakanmi, O., Beer, K., et al. (2011) Active starvation responses mediate antibiotic tolerance in biofilms and nutrient-limited bacteria. Science 334: 982-986.
94. Nystrom, T. (2004) Growth versus maintenance: a trade-off dictated by RNA polymerase availability and sigma factor competition? Mol Microbiol 54: 855-862.
95. Ogasawara, H., Yamamoto, K., and Ishihama, A. (2010a) Regulatory role of MlrA in transcription activation of csgD, the master regulator of biofilm formation in Escherichia coli. FEMS Microbiol Lett 312: 160-168.
96. Ogasawara, H., Yamada, K., Kori, A., Yamamoto, K., and Ishihama, A. (2010b) Regulation of the Escherichia coli csgD promoter: interplay between five transcription factors. Microbiology 156: 2470-2483.
97. Ogasawara, H., Yamamoto, K., and Ishihama, A. (2011) Role of the biofilm master regulator CsgD in cross-regulation between biofilm formation and flagellar synthesis. J Bacteriol 193: 2587-2597.
98. 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.
99. O'Toole, G.A. (2011) Microtiter dish biofilm formation assay. J Vis Exp 47: doi:103791/2437.
100. Paul, K., Nieto, V., Carlquist, W.C., Blair, D.F., and Harshey, R.M. (2010) The c-di-GMP binding protein YcgR controls flagellar motor direction and speed to affect chemotaxis by a 'backstop brake' mechanism. Mol Cell 38: 128- 139.
101. Pesavento, C., and Hengge, R. (2012) The global repressor FliZ antagonizes gene expression by sigmaS-containing RNA polymerase due to overlapping DNA binding specificity. Nucleic Acids Res 40: 4783-4793.
102. Pesavento, C., Becker, G., Sommerfeldt, N., Possling, A., Tschowri, N., Mehlis, A., and Hengge, R. (2008) Inverse regulatory coordination of motility and curlimediated adhesion in Escherichia coli. Genes Dev 22: 2434-2446.
103. Peterson, B.W., van der Mei, H.C., Sjollema, J., Busscher, H.J., and Sharma, P.K. (2013) A distinguishable role of eDNA in the viscoelastic relaxation of biofilms. MBio 4: e00497-13.
104. Pratt, L.A., and Kolter, R. (1998) Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili. Mol Microbiol 30: 285- 293.
105. Price, C.W. (2011) The general stress response in Bacillus subtilis and related Gram-positive bacteria. In Bacterial Stress Responses. Storz, G., and Hengge, R. (eds). Washington, DC: ASM press, pp. 301-318.
106. Prigent-Combaret, C., Brombacher, E., Vidal, O., Ambert, A., Lejeune, P., Landini, P., and Dorel, C. (2001) Complex regulatory network controls initial adhesion and biofilm formation in Escherichia coli via regulation of the csgD gene. J Bacteriol 183: 7213-7223.
107. Pruteanu, M., and Hengge-Aronis, R. (2002) The cellular level of the recognition factor RssB is rate-limiting for sigmaS proteolysis: implications for RssB regulation and signal transduction in sigmaS turnover in Escherichia coli. Mol Microbiol 45: 1701-1713.
108. Pultz, I.S., Christen, M., Kulasekara, H.D., Kennard, A., Kulasekara, B., and Miller, S.I. (2012) The response threshold of Salmonella PilZ domain proteins is determined by their binding affinities for c-di-GMP. Mol Microbiol 86: 1424-1440.
109. Rani, S.A., Pitts, B., Beyenal, H., Veluchamy, R.A., Lewandowski, Z., Davison, W.M., et al. (2007) Spatial patterns of DNA replication, protein synthesis, and oxygen concentration within bacterial biofilms reveal diverse physiological states. J Bacteriol 189: 4223-4233.
110. Ren, D., Bedzyk, L.A., Setlow, P., Thomas, S.M., Ye, R.W., and Wood, T.K. (2004) Gene expression in Bacillus subtilis surface biofilms with and without sporulation and the importance of yveR for biofilm maintenance. Biotechnol Bioeng 86: 344-364.
111. 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.
112. Ross, P., Weinhouse, H., Aloni, Y., Michaeli, D., Weinberger-Ohana, P., Mayer, R., et al. (1987) Regulation of cellulose synthesis in Acetobacter xylinum by cyclic diguanylic acid. Nature 325: 279-281.
113. Römling, U. (2005) Characterization of the rdar morphotype, a multicellular behaviour in Enterobacteriaceae. Cell Mol Life Sci 62: 1234-1246.
114. Römling, U., Sierralta, W.D., Eriksson, K., and Normark, S. (1998) Multicellular and aggregative behaviour of Salmonella typhimurium strains is controlled by mutations in the agfD promoter. Mol Microbiol 28: 249-264.
115. Römling, U., Rohde, M., Olsen, A., Normark, S., and Reinkoster, J. (2000) AgfD, the checkpoint of multicellular and aggregative behaviour in Salmonella typhimurium regulates at least two independent pathways. Mol Microbiol 36: 10-23.
116. Römling, U., Gomelsky, M., and Galperin, M.Y. (2005) C-di-GMP: the dawning of a novel bacterial signalling system. Mol Microbiol 57: 629-639.
117. Römling, U., Galperin, M.Y., and Gomelsky, M. (2013) Cyclic di-GMP: the first 25 years of a universal bacterial second messenger. Microbiol Mol Biol Rev 77: 1-52.
118. Schembri, M.A., Kjaergaard, K., and Klemm, P. (2003) Global gene expression in Escherichia coli biofilms. Mol Microbiol 48: 253-267.
119. Schirmer, T., and Jenal, U. (2009) Structural and mechanistic determinants of c-di-GMP signalling. Nat Rev Microbiol 7: 724-735.
120. Serra, D.O., Richter, A.M., and Hengge, R. (2013a) Cellulose as an architectural element in spatially structured Escherichia coli biofilms. J Bacteriol 195: 5540-5554.
121. Serra, D.O., Richter, A.M., Klauck, G., Mika, F., and Hengge, R. (2013b) Microanatomy at cellular resolution and spatial order of physiological differentiation in a bacterial biofilm. MBio 4: e103-e113.
122. Shimada, T., Fujita, N., Yamamoto, K., and Ishihama, A. (2011) Novel roles of cAMP receptor protein (CRP) in regulation of transport and metabolism of carbon sources. PLoS ONE 6: e20081.
123. Simm, R., Morr, M., Kader, A., Nimtz, M., and Romling, U. (2004) GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Mol Microbiol 53: 1123-1134.
124. Sommerfeldt, N., Possling, A., Becker, G., Pesavento, C., Tschowri, N., and Hengge, R. (2009) Gene expression patterns and differential input into curli fimbriae regulation of all GGDEF/EAL domain proteins in Escherichia coli. Microbiology 155: 1318-1331.
125. Soutourina, O., Kolb, A., Krin, E., Laurent-Winter, C., Rimsky, S., Danchin, A., and Bertin, P. (1999) Multiple control of flagellum biosynthesis in Escherichia coli: role of H-NS protein and the cyclic AMP-catabolite activator protein complex in transcription of the flhDC master operon. J Bacteriol 181: 7500-7508.
126. Spangler, C., Bohm, A., Jenal, U., Seifert, R., and Kaever, V. (2010) A liquid chromatography-coupled tandem mass spectrometry method for quantitation of cyclic di-guanosine monophosphate. J Microbiol Methods 81: 226-231.
127. Stewart, P.S., and Franklin, M.J. (2008) Physiological heterogeneity in biofilms. Nat Rev Microbiol 6: 199-210.
128. Stoodley, P., Sauer, K., Davies, D.G., and Costerton, J.W. (2002) Biofilms as complex differentiated communities. Annu Rev Microbiol 56: 187-209.
129. Storz, G., and Hengge, R. (eds) (2011) Bacterial Stress Responses. Washington, DC: ASM Press.
130. Thomason, M.K., Fontaine, F., De Lay, N., and Storz, G. (2012) A small RNA that regulates motility and biofilm formation in response to changes in nutrient availability in Escherichia coli. Mol Microbiol 84: 17-35.
131. Traxler, M.F., Zacharia, V.M., Marquardt, S., Summers, S.M., Nguyen, H.T., Stark, S.E., and Conway, T. (2011) Discretely calibrated regulatory loops controlled by ppGpp partition gene induction across the 'feast to famine' gradient in Escherichia coli. Mol Microbiol 79: 830-845.
132. 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.
133. Typas, A., Barembruch, C., Possling, A., and Hengge, R. (2007) Stationary phase reorganisation of the Escherichia coli transcription machinery by Crl protein, a fine-tuner of sigmas activity and levels. EMBO J 26: 1569-1578.
134. 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.
135. 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.
136. 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.
137. Wang, S., Fleming, R.T., Westbrook, E.M., Matsumura, P., and McKay, D.B. (2006) Structure of the Escherichia coli FlhDC complex, a prokaryotic heteromeric regulator of transcription. J Mol Biol 355: 798-808.
138. Weber, H., Polen, T., Heuveling, J., Wendisch, V.F., and Hengge, R. (2005) Genome-wide analysis of the general stress response network in Escherichia coli: sigmaSdependent genes, promoters, and sigma factor selectivity. J Bacteriol 187: 1591-1603.
139. Weber, H., Pesavento, C., Possling, A., Tischendorf, G., and Hengge, R. (2006) Cyclic-di-GMP-mediated signalling within the sigma network of Escherichia coli. Mol Microbiol 62: 1014-1034.
140. Werner, E., Roe, F., Bugnicourt, A., Franklin, M.J., Heydorn, A., Molin, S., et al. (2004) Stratified growth in Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 70: 6188-6196.
141. Williamson, K.S., Richards, L.A., Perez-Osorio, A.C., Pitts, B., McInnerney, K., Stewart, P.S., and Franklin, M.J. (2012) Heterogeneity in Pseudomonas aeruginosa biofilms includes expression of ribosome hibernation factors in the antibiotic-tolerant subpopulation and hypoxia-induced stress response in the metabolically active population. J Bacteriol 194: 2062-2073.
142. Wood, T.K., Gonzalez Barrios, A.F., Herzberg, M., and Lee, J. (2006) Motility influences biofilm architecture in Escherichia coli. Appl Microbiol Biotechnol 72: 361-367.
143. Yang, L., Hu, Y., Liu, Y., Zhang, J., Ulstrup, J., and Molin, S. (2011) Distinct roles of extracellular polymeric substances in Pseudomonas aeruginosa biofilm development. Environ Microbiol 13: 1705-1717.
144. Yildiz, F.H., and Schoolnik, G.K. (1999) Vibrio cholerae O1 El Tor: identification of a gene cluster required for the rugose colony type, exopolysaccharide production, chlorine resistance, and biofilm formation. Proc Natl Acad Sci USA 96: 4028-4033.
145. Zhao, K., Liu, M., and Burgess, R.R. (2007) Adaptation in bacterial flagellar and motility systems: from regulon members to 'foraging'-like behavior in E. coli. Nucleic Acids Res 35: 4441-4452.
146. Zogaj, X., Nimtz, M., Rohde, M., Bokranz, W., and 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.