1887

Chapter 10 : Hierarchical Control of rdar Morphotype Development of by Cyclic Di-GMP

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Ebook: Choose a downloadable PDF or ePub file. Chapter is a downloadable PDF file. File must be downloaded within 48 hours of purchase

Buy this Chapter
Digital (?) $15.00

Preview this chapter:
Zoom in
Zoomout

Hierarchical Control of rdar Morphotype Development of by Cyclic Di-GMP, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555816667/9781555814991_Chap10-1.gif /docserver/preview/fulltext/10.1128/9781555816667/9781555814991_Chap10-2.gif

Abstract:

This chapter describes in detail the role of bis-(3',5')-cyclic di-GMP (c-di-GMP) signaling in the expression of the rdar morphotype, one of the major targets of c-di-GMP signaling in serovar Typhimurium. It describes the impact of this multicellular morphotype and the complex molecular mechanisms by which it is regulated. Further, the chapter discusses the role of c-di-GMP in motility and characterizes the upcoming molecular mechanisms that tightly control the switch between the sedentary state and motility at various levels in the respective regulatory cascades. Initial characterization of the growth of serovar Typhimurium in rdar morphotype colonies on agar plates demonstrated that the formation of this morphotype represents a specific form of multicellular behavior (biofilm) in bacteria. An intrinsic characteristic of biofilm formation, the formation of a self-produced extracellular matrix, is required to construct the complex three dimensional architecture of the biofilm. Expression of the rdar morphotype is usually highly controlled in response to environmental conditions. With few exceptions, under laboratory conditions, the rdar morphotype is expressed on Luria broth agar plates without salt at temperatures below 30№C. Experiments in which , encoding a highly potent diguanylate cyclase (DGC), and STM3611, encoding a highly potent phosphodiesterase (PDE), were overexpressed first indicated c-di-GMP-dependent regulation of CsgD expression.

Citation: Römling U, Jonas K, Melefors Ö, Grantcharova N, Lamprokostopoulou A. 2010. Hierarchical Control of rdar Morphotype Development of by Cyclic Di-GMP, p 137-155. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch10

Key Concept Ranking

Type 1 Fimbriae
0.4464915
Coomassie Brilliant Blue
0.42255715
Scanning Electron Microscopy
0.42255715
Integral Membrane Proteins
0.4103663
0.4464915
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Image of Figure 1.
Figure 1.

Appearance of the rdar morphotype of serovar Typhimurium ATCC 14028. (A) rdar morphotype colonies among smooth colonies on Congo red agar plates. Streak-outs from the original serovar Typhimurium ATCC 14028 culture were grown for 24 h at 37°C on Congo red agar plates using Luria broth (LB) without salt as growth medium. The extracellular matrix produced by rdar colonies bind the dye Congo red, which leads to a red-colored colony with extended dimensions. (B) Scanning electron microscopic analysis of the extracellular matrix structure and cell organization of rdar type serovar Typhimurium ATCC 14028 (a Δ Δ mutant). The extracellular matrix surrounds the individual cell resembling a honeycomb-like structure. Magnification, X 15,000; bar, 2 µm. Picture taken by Manfred Rohde, Helmholtz Center for Infection Biology, Braunschweig, Germany. (C) rdar morphotype expression in liquid culture leads to cell clumping. Magnification, X∼473. (D) Differential expression of CsgD-GFP in rdar morphotype formation. GFP was fused to the open reading frame on its native chromosomal location (Grantcharova and Römling, unpublished). Cell clumping is associated with the expression of the master regulator of rdar morphotype formation, CsgD, in the cytoplasm, while single cells usually do not express CsgD. Cells were grown for 24 h at 28°C on LB without salt agar plates. Cells were stained with FM4-64 membrane stain. Bar, 2 μm.

Citation: Römling U, Jonas K, Melefors Ö, Grantcharova N, Lamprokostopoulou A. 2010. Hierarchical Control of rdar Morphotype Development of by Cyclic Di-GMP, p 137-155. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch10
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 2.
Figure 2.

rdar morphotype expression in serovar Typhimurium ATCC 14028. (A) Morphotypes of serovar Typhimurium expressing the extracellular matrix components curli fimbriae and cellulose. For pronounced visualization, strain MAE52, an ATCC 14028 derivative with semiconstitutive expression of the rdar morphotype, and respective mutants were used. MAE52 has a single point mutation in the promoter that confers threefold-enhanced transcription of which is RpoS and temperature independent ( ). (B) The transcriptional regulator CsgD positively regulates the expression of at least four extracellular matrix components in serovar Typhimurium, proteinaceous curli fimbriae, BapA, exopolysaccharide cellulose, and a capsule ( ). Thereby, CsgD activates the transcription of the target operons and The operon encodes CsgA and CsgB, major and minor structural components of curli fimbriae, respectively. The operon encodes the large surface protein BapA and its type I protein secretion apparatus. Expression of the DGC AdrA produces c-di-GMP required for posttranscriptional activation of cellulose biosynthesis. On the other hand, CsgD represses transcription of the operon, which leads to the activation of the divergently transcribed operon and expression of an O-antigen capsule.

Citation: Römling U, Jonas K, Melefors Ö, Grantcharova N, Lamprokostopoulou A. 2010. Hierarchical Control of rdar Morphotype Development of by Cyclic Di-GMP, p 137-155. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch10
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 3.
Figure 3.

Regulatory network of rdar morphotype expression in serovar Typhimurium with CsgD as central regulator. Regulation by c-di-GMP metabolic enzymes is shown in Fig. 5 . Expression of CsgD is positively (gray arrows) and negatively (black arrows) regulated by two-component systems (EnvZ/OmpR, CpxA/CpxR, and RcsCD/RcsBA), sigma factors and associated proteins (RpoS and Crl), transcriptional regulators (MlrA), and nucleoid-binding proteins (H-NS and IHF).

Citation: Römling U, Jonas K, Melefors Ö, Grantcharova N, Lamprokostopoulou A. 2010. Hierarchical Control of rdar Morphotype Development of by Cyclic Di-GMP, p 137-155. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch10
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 4.
Figure 4.

Panel of GGDEF-EAL domain proteins present in serovar Typhimurium. The domain structures of the 5 GGDEF, 7 EAL, and 7 GGDEF-EAL domain proteins are shown. The GGDEF domain proteins STM2410, STM2503, STM3375, and STM3615 do not show a complete signature of conserved amino acids in the GGDEF motif (as indicated in the figure by pale letters) and other signature motifs indicative for enzymatic activity, suggesting that DGC activity is missing. The EAL domain proteins STM1344, STM1697, STM2123, and STM3375 do not show a complete signature of conserved amino acids in the EAL motif (as indicated in the figure by pale letters) and other signature motifs indicative for enzymatic activity, suggesting that c-di-GMP-specific PDE activity is missing. Although STM3611 shows several deviations from the PDE signature motif, considerable c-di-GMP-specific PDE activity was observed ( ). Besides STM1344, STM1697, STM1703, and STM3611, the proteins are predicted to be integral membrane proteins, suggesting that the c-di-GMP signaling network responds mainly to external signals in serovar Typhimurium.

Citation: Römling U, Jonas K, Melefors Ö, Grantcharova N, Lamprokostopoulou A. 2010. Hierarchical Control of rdar Morphotype Development of by Cyclic Di-GMP, p 137-155. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch10
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 5.
Figure 5.

c-di-GMP metabolic network affecting expression of CsgD, the master regulator of rdar morphotype formation. At least eight GGDEF and/or EAL domain proteins are involved in the regulation of the rdar morphotype in serovar Typhimurium growing on agar plates ( ). STM2123, STM3388, and other unidentified DGCs produce c-di-GMP (indicated by dots). STM1703, STM4264, STM1827, and STM3611 lead to c-di-GMP degradation. STM4264 and STM1703 have the most drastic effect on CsgD expression (indicated by thick lines). STM4264 acts upstream of STM1703, since STM1703 can complement an STM4264 defect by downregulation of CsgD but not vice versa ( ). STM1827 and STM3611 have a less dramatic effect on CsgD expression. regulated on the transcriptional level by CsgD is necessary for cellulose biosynthesis and is partially involved in the production of curli fimbriae ( ). The EAL-like protein STM1344 does not have PDE activity but represses expression of the PDEs STM1703 and STM3611 ( ). STM1344 and STM3611 are direct targets of the carbon storage regulatory protein CsrA (42a). Thereby, CsrA represses expression of STM1344 and activates expression of STM3611.

Citation: Römling U, Jonas K, Melefors Ö, Grantcharova N, Lamprokostopoulou A. 2010. Hierarchical Control of rdar Morphotype Development of by Cyclic Di-GMP, p 137-155. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch10
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 6.
Figure 6.

c-di-GMP binding proteins identified in serovar Typhimurium. The PilZ domain is a c-di-GMP binding domain. The PilZ domain containing proteins STM1798 (YcgR) and BcsA have been identified in serovar Typhimurium, which regulate motility and perform cellulose biosynthesis, respectively. The PilZ domain containing protein YcgR regulates motility. Upon high c-di-GMP levels, YcgR binds c-di-GMP ( ) and presumably inhibits the flagellar motor function ( ). c-di-GMP is required for cellulose biosynthesis in serovar Typhimurium ( ). BcsA, the catalytic subunit of the cellulose synthase, contains a PilZ domain at the C terminus. As the PilZ domain of the cellulose synthase of has been demonstrated to bind c-di-GMP ( ), it is hypothesized that PilZ binds c-di-GMP, which allosterically activates cellulose biosynthesis in serovar Typhimurium.

Citation: Römling U, Jonas K, Melefors Ö, Grantcharova N, Lamprokostopoulou A. 2010. Hierarchical Control of rdar Morphotype Development of by Cyclic Di-GMP, p 137-155. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch10
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 7.
Figure 7.

Direct control of regulation of GGDEF-EAL domain proteins by the carbon storage regulator CsrA in serovar Typhimurium ATCC 14028 controls biofilm formation, motility, and invasion. CsrA directly represses the expression of the GGDEF-EAL protein STM3375 and the EAL-like domain proteins STM1344 and STM1697, whereas the PDE STM3611 is activated through CsrA. CsrA is predicted to inversely control rdar morphotype expression and motility through STM1344 and STM3611. CsrA is suggested to control invasion by regulating STM1697 and STM1987 by an unknown mechanism. CsrA regulates the expression of invasion genes ( ). CsrA controls its own activity by regulating STM3375, which in turn destabilizes the CsrB and CsrC sRNAs, the antagonists of CsrA activity ( ).

Citation: Römling U, Jonas K, Melefors Ö, Grantcharova N, Lamprokostopoulou A. 2010. Hierarchical Control of rdar Morphotype Development of by Cyclic Di-GMP, p 137-155. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch10
Permissions and Reprints Request Permissions
Download as Powerpoint

References

/content/book/10.1128/9781555816667.ch10
1. Aldridge, P.,, R. Paul,, P. Goymer,, P. Rainey, and, U. Jenal. 2003. Role of the GGDEF regulator PleD in polar development of Caulobacter crescentus. Mol. Microbiol. 47:16951708.
2. Altier, C.,, M. Suyemoto, and, S. D. Lawhon. 2000. Regulation of Salmonella enterica serovar Typhimurium invasion genes by csrA. Infect. Immun. 68:67906797.
3. Altier, C.,, M. Suyemoto,, A. I. Ruiz,, K. D. Burnham, and, R. Maurer. 2000. Characterization of two novel regulatory genes affecting Salmonella invasion gene expression. Mol. Microbiol. 35:635646.
4. Amikam, D., and, M. Y. Galperin. 2006. PilZ domain is part of the bacterial c-di-GMP binding protein. Bioinformatics 22:36.
5. Ausmees, N.,, R. Mayer,, H. Weinhouse,, G. Volman,, D. Amikam,, M. Benziman, and, M. Lindberg. 2001. Genetic data indicate that proteins containing the GGDEF domain possess diguanylate cyclase activity. FEMS Microbiol. Lett. 204:163167.
6. Austin, J. W.,, G. Sanders,, W. W. Kay, and, S. K. Collinson. 1998. Thin aggregative fimbriae enhance Salmonella enteritidis biofilm formation. FEMS Microbiol. Lett. 162:295301.
7. Babitzke, P., and, T. Romeo. 2007. CsrB sRNA family: sequestration of RNA-binding regulatory proteins. Curr. Opin. Microbiol. 10:156163.
8. Barak, J. D.,, L. Gorski,, P. Naraghi-Arani, and, A. O. Charkowski. 2005. Salmonella enterica virulence genes are required for bacterial attachment to plant tissue. Appl. Environ. Microbiol. 71:56855691.
9. Barak, J. D.,, C. E. Jahn,, D. L. Gibson, and, A. O. Charkowski. 2007. The role of cellulose and O-antigen capsule in the colonization of plants by Salmonella enterica. Mol. Plant-Microbe Interact. 20:10831091.
10. Barnhart, M. M.,, J. Lynem, and, M. R. Chapman. 2006. GlcNAc-6P levels modulate the expression of curli fibers by Escherichia coli. J. Bacteriol. 188:52125219.
11. Beyhan, S.,, A. D. Tischler,, A. Camilli, and, F. H. Yildiz. 2006. Transcriptome and phenotypic responses of Vibrio cholerae to increased cyclic di-GMP level. J. Bacteriol. 188:36003613.
12. Bokranz, W.,, X. Wang,, H. Tschäpe, and, U. Römling. 2005. Expression of cellulose and curli fimbriae by Escherichia coli isolated from the gastrointestinal tract. J. Med. Microbiol. 54:11711182.
13. Brombacher, E.,, A. Baratto,, C. Dorel, and, P. Landini. 2006. Gene expression regulation by the curli activator CsgD protein: modulation of cellulose biosynthesis and control of negative determinants for microbial adhesion. J. Bacteriol. 188:20272037.
14. Brombacher, E.,, C. Dorel,, A. J. Zehnder, and, P. Landini. 2003. The curli biosynthesis regulator CsgD co-ordinates the expression of both positive and negative determinants for biofilm formation in Escherichia coli. Microbiology 149:28472857.
15. Brown, P. K.,, C. M. Dozois,, C. A. Nickerson,, A. Zuppardo,, J. Terlonge, and, R. Curtiss III. 2001. MlrA, a novel regulator of curli (AgF) and extracellular matrix synthesis by Escherichia coli and Salmonella enterica serovar Typhimurium. Mol. Microbiol. 41:349363.
16. Christen, M.,, B. Christen,, M. Folcher,, A. Schauerte, and, U. Jenal. 2005. Identification and characterization of a cyclic di-GMP-specific phosphodiesterase and its allosteric control by GTP. J. Biol. Chem. 280:3082930837.
17. Collinson, S. K.,, P. C. Doig,, J. L. Doran,, S. Clouthier,, T. J. Trust, and, W. W. Kay. 1993. Thin, aggregative fimbriae mediate binding of Salmonella enteritidis to fibronectin. J. Bacteriol. 175:1218.
18. Collinson, S. K.,, L. Emody,, K. H. Muller,, T. J. Trust, and, W. W. Kay. 1991. Purification and characterization of thin, aggregative fimbriae from Salmonella enteritidis. J. Bacteriol. 173:47734781.
19. Collinson, S. K.,, L. Emody,, T. J. Trust, and, W. W. Kay. 1992. Thin aggregative fimbriae from diarrheagenic Escherichia coli. J. Bacteriol. 174:44904495.
20. Costerton, J. W.,, Z. Lewandowski,, D. E. Caldwell,, D. R. Korber, and, H. M. Lappin-Scott. 1995. Microbial biofilms. Annu. Rev. Microbiol. 49:711745.
21. D’Argenio,, D. A.,, M. W. Calfee,, P. B. Rainey, and, E. C. Pesci. 2002. Autolysis and autoaggregation in Pseudomonas aeruginosa colony morphology mutants. J. Bacteriol. 184:64816489.
22. Davidson, C. J.,, A. P. White, and, M. G. Surette. 2008. Evolutionary loss of the rdar morphotype in Salmonella as a result of high mutation rates during laboratory passage. ISME J. 2:293307.
23. Drenkard, E., and, F. M. Ausubel. 2002. Pseudomonas biofilm formation and antibiotic resistance are linked to phenotypic variation. Nature 416:740743.
24. Fong, J. C., and, F. H. Yildiz. 2008. Interplay between cyclic AMP-cyclic AMP receptor protein and cyclic di-GMP signaling in Vibrio cholerae biofilm formation. J. Bacteriol. 190:66466659.
25. Fortune, D. R.,, M. Suyemoto, and, C. Altier. 2006. Identification of CsrC and characterization of its role in epithelial cell invasion in Salmonella enterica serovar Typhimurium. Infect. Immun. 74:331339.
26. Galperin, M. Y.,, A. N. Nikolskaya, and, E. V. Koonin. 2001. Novel domains of the prokaryotic two-component signal transduction systems. FEMS Microbiol. Lett. 203:1121.
27. Garcia, B.,, C. Latasa,, C. Solano,, F. G. Portillo,, C. Gamazo, and, I. Lasa. 2004. Role of the GGDEF protein family in Salmonella cellulose biosynthesis and biofilm formation. Mol. Microbiol. 54:264277.
28. Gerstel, U.,, A. Kolb, and, U. Roömling. 2006. Regulatory components at the csgD promoter—additional roles for OmpR and integration host factor and role of the 5′ untranslated region. FEMS Microbiol. Lett. 261:109117.
29. Gerstel, U.,, C. Park, and, U. Roömling. 2003. Complex regulation of csgD promoter activity by global regulatory proteins. Mol. Microbiol. 49:639654.
30. Gerstel, U., and, U. Roömling. 2001. Oxygen tension and nutrient starvation are major signals that regulate agfD promoter activity and expression of the multicellular morphotype in Salmonella typhimurium. Environ. Microbiol. 3:638648.
31. Gerstel, U., and, U. Roömling. 2003. The csgD promoter, a control unit for biofilm formation in Salmonella typhimurium. Res. Microbiol. 154:659667.
32. Gibson, D. L.,, A. P. White,, S. D. Snyder,, S. Martin,, C. Heiss,, P. Azadi,, M. Surette, and, W. W. Kay. 2006. Salmonella produces an O-antigen capsule regulated by AgfD and important for environmental persistence. J. Bacteriol. 188:77227730.
33. Gophna, U.,, M. Barlev,, R. Seijffers,, T. A. Oelschlager,, J. Hacker, and, E. Z. Ron. 2001. Curli fibers mediate internalization of Escherichia coli by eukaryotic cells. Infect. Immun. 69:26592665.
34. Gronewold, T. M., and, D. Kaiser. 2001. The act operon controls the level and time of C-signal production for Myxococcus xanthus development. Mol. Microbiol. 40 744756.
35. Gualdi, L.,, L. Tagliabue, and, P. Landini. 2007. Biofilm formation-gene expression relay system in Escherichia coli: modulation of σS-dependent gene expression by the CsgD regulatory protein via σS protein stabilization. J. Bacteriol. 189:80348043.
36. Hecht, G. B., and, A. Newton. 1995. Identification of a novel response regulator required for the swarmer-to-stalked-cell transition in Caulobacter crescentus. J. Bacteriol. 177:62236229.
37. Herwald, H.,, M. Morgelin,, A. Olsen,, M. Rhen,, B. Dahlback,, W. Muller-Esterl, and, L. Bjorck. 1998. Activation of the contact-phase system on bacterial surfaces—a clue to serious complications in infectious diseases. Nat. Med. 4:298302.
38. Hisert, K. B.,, M. MacCoss,, M. U. Shiloh,, K. H. Darwin,, S. Singh,, R. A. Jones,, S. Ehrt,, Z. Zhang,, B. L. Gaffney,, S. Gandotra,, D. W. Holden,, D. Murray, and, C. Nathan. 2005. A glutamate-alanine-leucine (EAL) domain protein of Salmonella controls bacterial survival in mice, antioxidant defence and killing of macrophages: role of cyclic diGMP. Mol. Microbiol. 56:12341245.
39. Houslay, M. D., and, G. Milligan. 1997. Tailoring cAMP-signalling responses through isoform multiplicity. Trends Biochem. Sci. 22:217224.
40. Huang, Y. H.,, L. Ferrieres, and, D. J. Clarke. 2006. The role of the Rcs phosphorelay in Enterobacteriaceae. Res. Microbiol. 157:206212.
41. Jackson, D. W.,, J. W. Simecka, and, T. Romeo. 2002. Catabolite repression of Escherichia coli biofilm formation. J. Bacteriol. 184:34063410.
42. Jonas, K.,, A. N. Edwards,, R. Simm,, T. Romeo,, U. Römling, and, Ö. Melefors. 2008. The RNA binding protein CsrA controls cyclic di-GMP metabolism by directly regulating the expression of GGDEF proteins. Mol. Microbiol. 70:236257.
43. Jonas,, K.,, A. N. Edwards,, I. Ahmad,, T. Romeo,, U. Römling, and, O. Melefors. 2009. Complex regulatory network encompassing the Csr, c-di-GMP and motility systems of Salmonella Typhimurium. Environ. Microbiol., in press.
44. Jonas, K.,, O. Melefors, and, U. Römling. 2009. Regulation of c-di-GMP metabolism in biofilms. Future Microbiol. 4:341358.
45. Jonas, K.,, H. Tomenius,, A. Kader,, S. Normark,, U. Römling,, L. M. Belova, and, O. Melefors. 2007. Roles of curli, cellulose and BapA in Salmonella biofilm morphology studied by atomic force microscopy. BMC Microbiol. 7:70.
46. Jonas, K.,, H. Tomenius,, U. Römling,, D. Georgellis, and, O. Melefors. 2006. Identification of YhdA as a regulator of the Escherichia coli carbon storage regulation system. FEMS Microbiol. Lett. 264:232237.
47. Jones, H. A.,, J. W. Lillard, Jr., and, R. D. Perry. 1999. HmsT, a protein essential for expression of the haemin storage (Hms+) phenotype of Yersinia pestis. Microbiology 145:21172128.
48. Joseph, B.,, S. K. Otta, and, I. Karunasagar. 2001. Biofilm formation by Salmonella spp. on food contact surfaces and their sensitivity to sanitizers. Int. J. Food Microbiol. 64:367372.
49. Jubelin, G.,, A. Vianney,, C. Beloin,, J. M. Ghigo,, J. C. Lazzaroni,, P. Lejeune, and, C. Dorel. 2005. CpxR/OmpR interplay regulates curli gene expression in response to osmolarity in Escherichia coli. J. Bacteriol. 187:20382049.
50. Kader, A.,, R. Simm,, U. Gerstel,, M. Morr, and, U. Römling. 2006. Hierarchical involvement of various GGDEF domain proteins in rdar morphotype development of Salmonella enterica serovar Typhimurium. Mol. Microbiol. 60:602616.
51. Kalivoda, E. J.,, N. A. Stella,, D. M. O’Dee,, G. J. Nau, and, R. M. Shanks. 2008. The cyclic AMP-dependent catabolite repression system of Serratia marcescens mediates biofilm formation through regulation of type 1 fimbriae. Appl. Environ. Microbiol. 74:34613470.
52. Klausen, M.,, A. Aaes-Jorgensen,, S. Molin, and, T. Tolker-Nielsen. 2003. Involvement of bacterial migration in the development of complex multicellular structures in Pseudomonas aeruginosa biofilms. Mol. Microbiol. 50:6168.
53. Ko, M., and, C. Park. 2000. Two novel flagellar components and H-NS are involved in the motor function of Escherichia coli. J. Mol. Biol. 303:371382.
54. Kulesekara, H.,, V. Lee,, A. Brencic,, N. Liberati,, J. Urbach,, S. Miyata,, D. G. Lee,, A. N. Neely,, M. Hyodo,, Y. Hayakawa,, F. M. Ausubel, and, S. Lory. 2006. Analysis of Pseudomonas aeruginosa diguanylate cyclases and phosphodiesterases reveals a role for bis-(3′-5′)-cyclic-GMP in virulence. Proc. Natl. Acad. Sci. USA 103:28392844.
55. Lamprokostopoulou,, A.,, C. Monteiro,, M. Rhen, and, U. Römling. 2009. Cyclic di-GMP signalling controls virulence properties of Salmonella enterica serovar Typhimurium at the mucosal lining. Environ. Microbiol., in press.
56. Lapidot, A.,, U. Römling, and, S. Yaron. 2006. Biofilm formation and the survival of Salmonella Typhimurium on parsley. Int. J. Food Microbiol. 109:229233.
57. Lapouge, K.,, M. Schubert,, F. H. Allain, and, D. Haas. 2008. Gac/Rsm signal transduction pathway of gammaproteobacteria: from RNA recognition to regulation of social behaviour. Mol. Microbiol. 67:241253.
58. Latasa, C.,, A. Roux,, A. Toledo-Arana,, J. M. Ghigo,, C. Gamazo,, J. R. Penades, and, I. Lasa. 2005. BapA, a large secreted protein required for biofilm formation and host colonization of Salmonella enterica serovar Enteritidis. Mol. Microbiol. 58:13221339.
59. Lawhon, S. D.,, J. G. Frye,, M. Suyemoto,, S. Porwollik,, M. McClelland, and, C. Altier. 2003. Global regulation by CsrA in Salmonella typhimurium. Mol. Microbiol. 48:16331645.
60. Ledeboer, N. A.,, J. G. Frye,, M. McClelland, and, B. D. Jones. 2006. Salmonella enterica serovar Typhimurium requires the Lpf, Pef, and Tafi fimbriae for biofilm formation on HEp-2 tissue culture cells and chicken intestinal epithelium. Infect. Immun. 74:31563169.
61. Ledeboer, N. A., and, B. D. Jones. 2005. Exopolysaccharide sugars contribute to biofilm formation by Salmonella enterica serovar Typhimurium on HEp-2 cells and chicken intestinal epithelium. J. Bacteriol. 187:32143226.
62. Liang, W.,, A. J. Silva, and, J. A. Benitez. 2007. The cyclic AMP receptor protein modulates colonial morphology in Vibrio cholerae. Appl. Environ. Microbiol. 73:74827487.
63. Liu, M. Y.,, G. Gui,, B. Wei,, J. F. Preston III,, L. Oakford,, U. Yuksel,, D. P. Giedroc, and, T. Romeo. 1997. The RNA molecule CsrB binds to the global regulatory protein CsrA and antagonizes its activity in Escherichia coli. J. Biol. Chem. 272:1750217510.
64. Lucchetti-Miganeh,, C.,, E. Burrowes,, C. Baysse, and, G. Ermel. 2008. The post-transcriptional regulator CsrA plays a central role in the adaptation of bacterial pathogens to different stages of infection in animal hosts. Microbiology 154:1629.
65. Minasov, G.,, S. Padavattan,, L. Shuvalova,, J. S. Brunzelle,, D. J. Miller,, A. Basle,, C. Massa,, F. R. Collart,, T. Schirmer, and, W. F. Anderson. 2009. Crystal structures of YkuI and its complex with second messenger cyclic di-GMP suggest catalytic mechanism of phosphodiester bond cleavage by EAL domains. J. Biol. Chem. 284:1317413184.
66. Ogasawara, H.,, A. Hasegawa,, E. Kanda,, T. Miki,, K. Yamamoto, and, A. Ishihama. 2007. Genomic SELEX search for target promoters under the control of the PhoQP-RstBA signal relay cascade. J. Bacteriol. 189:47914799.
67. Olsen, A.,, A. Jonsson, and, S. Normark. 1989. Fibronectin binding mediated by a novel class of surface organelles on Escherichia coli. Nature 338:652655.
68. Olsen, A.,, M. J. Wick,, M. Morgelin, and, L. Bjorck. 1998. Curli, fibrous surface proteins of Escherichia coli, interact with major histocompatibility complex class I molecules. Infect. Immun. 66:944949.
69. Paul, R.,, S. Weiser,, N. C. Amiot,, C. Chan,, T. Schirmer,, B. Giese, and, U. Jenal. 2004. Cell cycle-dependent dynamic localization of a bacterial response regulator with a novel diguanylate cyclase output domain. Genes Dev. 18:715727.
70. Pernestig, A. K.,, D. Georgellis,, T. Romeo,, K. Suzuki,, H. Tomenius,, S. Normark, and, O. Melefors. 2003. The Escherichia coli BarA-UvrY two-component system is needed for efficient switching between glycolytic and gluconeogenic carbon sources. J. Bacteriol. 185:843853.
71. Pesavento, C.,, G. Becker,, N. Sommerfeldt,, A. Possling,, N. Tschowri,, A. Mehlis, and, R. Hengge. 2008. Inverse regulatory coordination of motility and curli-mediated adhesion in Escherichia coli. Genes Dev. 22:24342446.
72. Rao, F.,, Y. Yang,, Y. Qi, and, Z. X. Liang. 2008. Catalytic mechanism of cyclic di-GMP-specific phosphodiesterase: a study of the EAL domain-containing RocR from Pseudomonas aeruginosa. J. Bacteriol. 190:36223631.
73. Rice, P. A. 1997. Making DNA do a U-turn: IHF and related proteins. Curr. Opin. Struct. Biol. 7:8693.
74. Robbe-Saule,, V.,, V. Jaumouille,, M. C. Prevost,, S. Guadagnini,, C. Talhouarne,, H. Mathout,, A. Kolb, and, F. Norel. 2006. Crl activates transcription initiation of RpoS-regulated genes involved in the multicellular behavior of Salmonella enterica serovar Typhimurium. J. Bacteriol. 188:39833994.
75. Romeo, T. 1998. Global regulation by the small RNA-binding protein CsrA and the non-coding RNA molecule CsrB. Mol. Microbiol. 29:13211330.
76. Romeo, T.,, M. Gong,, M. Y. Liu, and A. M. Brun-Zinkernagel. 1993. Identification and molecular characterization of csrA, a pleiotropic gene from Escherichia coli that affects glycogen biosynthesis, gluconeogenesis, cell size, and surface properties. J. Bacteriol. 175:47444755.
77. Roömling, U. 2005. Characterization of the rdar morphotype, a multicellular behaviour in Enterobacteriaceae. Cell. Mol. Life Sci. 62:12341246.
78. Roömling, U. 2009. Cyclic di-GMP (c-di-GMP) goes into host cells—c-di-GMP signaling in the obligate intracellular pathogen Anaplasma phagocytophilum. J. Bacteriol. 191:683686.
79. Roömling, U.,, Z. Bian,, M. Hammar,, W. D. Sierralta, and, S. Normark. 1998. Curli fibers are highly conserved between Salmonella typhimurium and Escherichia coli with respect to operon structure and regulation. J. Bacteriol. 180:722731.
80. Roömling, U.,, W. Bokranz,, W. Rabsch,, X. Zogaj,, M. Nimtz, and, H. Tschaåpe. 2003. Occurrence and regulation of the multicellular morphotype in Salmonella serovars important in human disease. Int. J. Med. Microbiol. 293:273285.
81. Roömling, U.,, M. Gomelsky, and, M. Y. Galperin. 2005. c-di-GMP: the dawning of a novel bacterial signalling system. Mol. Microbiol. 57:629639.
82. Ræmling, U.,, D. Pesen, and, S. Yaron. 2007. Biofilms of Salmonella enterica, p. 127-145. In M. Rhen,, D. Maskell,, P. Mastroeni, and, J. Threlfall. (ed.), Salmonella Molecular Biology and Pathogenesis. Horizon Press, Norfolk, United Kingdom.
83. Ræmling, U., and, M. Rohde. 1999. Flagella modulate the multicellular behavior of Salmonella typhimurium on the community level. FEMS Microbiol. Lett. 180:91102.
84. Roömling, U.,, M. Rohde,, A. Olsen,, S. Normark, and, J. Reinkoæster. 2000. AgfD, the checkpoint of multicellular and aggregative behaviour in Salmonella typhimurium regulates at least two independent pathways. Mol. Microbiol. 36:1023.
85. Roömling, U.,, W. D. Sierralta,, K. Eriksson, and, S. Normark. 1998. Multicellular and aggregative behaviour of Salmonella typhimurium strains is controlled by mutations in the agfD promoter. Mol. Microbiol. 28:249264.
86. Ryan, R. P.,, Y. Fouhy,, J. F. Lucey,, B. L. Jiang,, Y. Q. He,, J. X. Feng,, J. L. Tang, and, J. M. Dow. 2007. Cyclic di-GMP signalling in the virulence and environmental adaptation of Xanthomonas campestris. Mol. Microbiol. 63:429442.
87. Ryjenkov, D. A.,, R. Simm,, U. Roömling, and, M. Gomelsky. 2006. The PilZ domain is a receptor for the second messenger c-di-GMP. The PilZ domain protein YcgR controls motility in enterobacteria. J. Biol. Chem. 281:3031030314.
88. Ryjenkov, D. A.,, M. Tarutina,, O. V. Moskvin, and M. Gomelsky. 2005. Cyclic diguanylate is a ubiquitous signaling molecule in bacteria: insights into biochemistry of the GGDEF protein domain. J. Bacteriol. 187:17921798.
89. Scher, K.,, U. Roömling, and, S. Yaron. 2005. Effect of heat, acidification, and chlorination on Salmonella enterica serovar Typhimurium cells in a biofilm formed at the air-liquid interface. Appl. Environ. Microbiol. 71:11631168.
90. Schmidt, A. J.,, D. A. Ryjenkov, and, M. Gomelsky. 2005. The ubiquitous protein domain EAL is a cyclic diguanylate-specific phosphodiesterase: enzymatically active and inactive EAL domains. J. Bacteriol. 187:47744781.
91. Simm, R.,, A. Lusch,, A. Kader,, M. Andersson, and, U. Roömling. 2007. Role of EAL-containing proteins in multicellular behavior of Salmonella enterica serovar Typhimurium. J. Bacteriol. 189:36133623.
92. Simm, R.,, M. Morr,, A. Kader,, M. Nimtz, and, U. Roömling. 2004. GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Mol. Microbiol. 53:11231134.
93. Simm, R.,, U. Remminghorst,, I. Ahmad,, K. Zakikhany, and, U. Roömling. 2009. A role for the EAL-like protein STM1344 in regulation of CsgD expression and motility in Salmonella enterica serovar Typhimurium. J. Bacteriol. 191:39283937.
94. Solano, C.,, B. Garcia,, J. Valle,, C. Berasain,, J. M. Ghigo,, C. Gamazo, and, I. Lasa. 2002. Genetic analysis of Salmonella enteritidis biofilm formation: critical role of cellulose. Mol. Microbiol. 43:793808.
95. Sukupolvi, S.,, A. Edelstein,, M. Rhen,, S. J. Normark, and, J. D. Pfeifer. 1997. Development of a murine model of chronic Salmonella infection. Infect. Immun. 65:838842.
96. Suzuki, K.,, P. Babitzke,, S. R. Kushner, and, T. Romeo. 2006. Identification of a novel regulatory protein (CsrD) that targets the global regulatory RNAs CsrB and CsrC for degradation by RNase E. Genes Dev. 20:26052617.
97. Tabak, M.,, K. Scher,, E. Hartog,, U. Roömling,, K. R. Matthews,, M. L. Chikindas, and, S. Yaron. 2006. The effect of triclosan on Salmonella Typhimurium at different growth stages. FEMS Microbiol. Lett. 267:200206.
98. Tal, R.,, H. C. Wong,, R. Calhoon,, D. Gelfand,, A. L. Fear,, G. Volman,, R. Mayer,, P. Ross,, D. Amikam,, H. Weinhouse,, A. Cohen,, S. Sapir,, P. Ohana, and, M. Benziman. 1998. Three cdg operons control cellular turnover of cyclic di-GMP in Acetobacter xylinum: genetic organization and occurrence of conserved domains in isoenzymes. J. Bacteriol. 180:44164425.
99. Tamayo, R.,, J. T. Pratt, and, A. Camilli. 2007. Roles of cyclic diguanylate in the regulation of bacterial pathogenesis. Annu. Rev. Microbiol. 61:131148.
100. Tamayo, R.,, A. D. Tischler, and, A. Camilli. 2005. The EAL domain protein VieA is a cyclic diguanylate phosphodiesterase. J. Biol. Chem. 280:3332433330.
101. Teplitski, M.,, R. I. Goodier, and, B. M. Ahmer. 2003. Pathways leading from BarA/SirA to motility and virulence gene expression in Salmonella. J. Bacteriol. 185:72577265.
102. Thormann, K. M.,, S. Duttler,, R. M. Saville,, M. Hyodo,, S. Shukla,, Y. Hayakawa, and, A. M. Spormann. 2006. Control of formation and cellular detachment from Shewanella oneidensis MR-1 biofilms by cyclic di-GMP. J. Bacteriol. 188:26812691.
103. Tukel, C.,, M. Raffatellu,, A. D. Humphries,, R. P. Wilson,, H. L. Andrews-Polymenis,, T. Gull,, J. F. Figueiredo,, M. H. Wong,, K. S. Michelsen,, M. Akcelik,, L. G. Adams, and, A. J. Baumler. 2005. CsgA is a pathogen-associated molecular pattern of Salmonella enterica serotype Typhimurium that is recognized by Toll-like receptor 2. Mol. Microbiol. 58:289304.
104. Wang, X.,, A. K. Dubey,, K. Suzuki,, C. S. Baker,, P. Babitzke, and, T. Romeo. 2005. CsrA post-transcriptionally represses pgaABCD, responsible for synthesis of a biofilm polysaccharide adhesin of Escherichia coli. Mol. Microbiol. 56:16481663.
105. Wang, X.,, M. Rochon,, A. Lamprokostopoulou,, H. Lünsdorf,, M. Nimtz, and, U. Römling. 2006. Impact of biofilm matrix components on interaction of commensal Escherichia coli with the gastrointestinal cell line HT-29. Cell. Mol. Life Sci. 63:23522363.
106. Weber, H.,, C. Pesavento,, A. Possling,, G. Tischendorf, and, R. Hengge. 2006. Cyclic-di-GMP-mediated signalling within the sigma network of Escherichia coli. Mol. Microbiol. 62:10141034.
107. Wei, B. L.,, A. M. Brun-Zinkernagel,, J. W. Simecka,, B. M. Pruss,, P. Babitzke, and, T. Romeo. 2001. Positive regulation of motility and flhDC expression by the RNA-binding protein CsrA of Escherichia coli. Mol. Microbiol. 40:245256.
108. Weilbacher, T.,, K. Suzuki,, A. K. Dubey,, X. Wang,, S. Gudapaty,, I. Morozov,, C. S. Baker,, D. Georgellis,, P. Babitzke, and, T. Romeo. 2003. A novel sRNA component of the carbon storage regulatory system of Escherichia coli. Mol. Microbiol. 48:657670.
109. White, A. P.,, D. L. Gibson,, S. K. Collinson,, P. A. Banser, and, W. W. Kay. 2003. Extracellular polysaccharides associated with thin aggregative fimbriae of Salmonella enterica serovar Enteritidis. J. Bacteriol. 185:53985407.
110. White, A. P.,, D. L. Gibson,, G. A. Grassl,, W. W. Kay,, B. B. Finlay,, B. A. Vallance, and, M. G. Surette. 2008. Aggregation via the red, dry, and rough morphotype is not a virulence adaptation in Salmonella enterica serovar Typhimurium. Infect. Immun. 76:10481058.
111. White, A. P.,, D. L. Gibson,, W. Kim,, W. W. Kay, and, M. G. Surette. 2006. Thin aggregative fimbriae and cellulose enhance long-term survival and persistence of Salmonella. J. Bacteriol. 188:32193227.
112. Winfield, M. D., and, E. A. Groisman. 2003. Role of nonhost environments in the lifestyles of Salmonella and Escherichia coli. Appl. Environ. Microbiol. 69:36873694.
113. Wolfe, A. J., and, K. L. Visick. 2008. Get the message out: cyclic-di-GMP regulates multiple levels of flagellum-based motility. J. Bacteriol. 190:463475.
114. Wozniak, C. E.,, C. Lee, and, K. T. Hughes. 2008. T-POP array identifies EcnR and PefI-SrgD as novel regulators of flagellar gene expression. J. Bacteriol. 191:14981508.
115. Zogaj, X.,, W. Bokranz,, M. Nimtz, and, U. Römling. 2003. Production of cellulose and curli fimbriae by members of the family Enterobacteriaceae isolated from the human gastrointestinal tract. Infect. Immun. 71:41514158.
116. Zogaj, X.,, M. Nimtz,, M. Rohde,, W. Bokranz, and, U. Römling. 2001. The multicellular morphotypes of Salmonella typhimurium and Escherichia coli produce cellulose as the second component of the extracellular matrix. Mol. Microbiol. 39:14521463.

Tables

Generic image for table
Table 1

Characteristics of GGDEF-EAL domain proteins affecting CsgD expression

Citation: Römling U, Jonas K, Melefors Ö, Grantcharova N, Lamprokostopoulou A. 2010. Hierarchical Control of rdar Morphotype Development of by Cyclic Di-GMP, p 137-155. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch10

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error