1887

Chapter 16 : Role of Cyclic Di-GMP in the Regulatory Networks of

Author: Regine Hengge1
VIEW AFFILIATIONS HIDE AFFILIATIONS
Affiliations: 1: Institut für Biologie–Mikrobiologie, Freie Universität Berlin, 14195 Berlin, Germany
Content Type: Monograph
Publication Year: 2010

Category: Microbial Genetics and Molecular Biology

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

Preview this chapter:
Preview Magnify
Zoom in
Zoomout

Role of Cyclic Di-GMP in the Regulatory Networks of , Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555816667/9781555814991_Chap16-1.gif /docserver/preview/fulltext/10.1128/9781555816667/9781555814991_Chap16-2.gif

Abstract:

This chapter provides an integrative picture that reflects general principles of cyclic di-GMP (c-di-GMP) signaling as well as specific molecular functions of the 29 GGDEF/EAL domain proteins of and serves as a framework to elucidate the multiple functions of c-di-GMP signaling in a well-characterized model organism. is an environmentally versatile gram-negative bacterium that belongs to the gamma-proteobacteria and comes in a wide variety of strains that include commensals as well as important pathogens. The genomics era has revealed a striking abundance of genes encoding GGDEF and EAL domains in the genomes of many bacterial species (genes encoding HD-GYP domains are less frequent but can also be present several times in certain genomes). Functional sequestration and local operation of certain c-di-GMP control modules based on direct interactions in protein complexes can open new pathways for evolution. With a wealth of genome sequences now available, it has become apparent that c-di-GMP signaling indeed undergoes rapid evolution. Closely related species and even strains of the same species exhibit different sets of GGDEF/EAL domain proteins and use orthologs of these proteins in different regulatory circuits, suggesting that horizontal gene transfer and changes in regulation of expression are crucial for the rapid evolution of c-di-GMP signaling.

Citation: Hengge R. 2010. Role of Cyclic Di-GMP in the Regulatory Networks of , p 230-252. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch16
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Role of Cyclic Di-GMP in the Regulatory Networks of Escherichia coli
[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555816667.ch16-1,webId=/content/author/10.1128/9781555816667.ch16-1,properties={foaf_givenname=Regine, foaf_name=Regine Hengge, foaf_surname=Hengge, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555816667.ch16-aff1]]}]]
Citation: Hengge R. 2010. Role of Cyclic Di-GMP in the Regulatory Networks of , p 230-252. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch16
/content/10.1128/9781555816667.ch16.ch16fig01
Figure 1.
Growth phases and corresponding master regulators in K-12. In a culture of the K-12 strain W3110 growing in complex Luria-Bertani medium (LB), three growth phases can be distinguished: exponential or log phase (A), postexponential phase (B), and stationary phase (C). In the first part of the postex-ponential phase (starting at an optical density [OD] of approximately 0.3), the flagellar master regulator FlhDC and, therefore, flagella are expressed, but later on, further expression of FlhDC is shut down and existing FlhDC is degraded. As a consequence, further synthesis of flagella (and other proteins under FlhDC control) also comes to an end, but assembled flagella are active and cells are highly motile. In parallel, the master regulator of the stationary phase, σ, begins to accumulate but initially is only slowly assembling into active RNAP holoenzyme (Eσ). Upon entry into the stationary phase (at an OD of approximately 3), the regulator CsgD is induced, which is essential for the expression of adhesive curli fimbriae and other biofilm-related functions. Note that only relative amounts of the various regulatory proteins or complexes are shown, which cannot be compared directly. OD (578 nm), optical density of the culture measured at 578 nm; ON, overnight, i.e., at approximately 24 h. For further details and references, see the text.
10.1128/9781555816667/f0231-01_thmb.gif
10.1128/9781555816667/f0231-01.gif
Image of Figure 1.
Figure 1.

Growth phases and corresponding master regulators in K-12. In a culture of the K-12 strain W3110 growing in complex Luria-Bertani medium (LB), three growth phases can be distinguished: exponential or log phase (A), postexponential phase (B), and stationary phase (C). In the first part of the postex-ponential phase (starting at an optical density [OD] of approximately 0.3), the flagellar master regulator FlhDC and, therefore, flagella are expressed, but later on, further expression of FlhDC is shut down and existing FlhDC is degraded. As a consequence, further synthesis of flagella (and other proteins under FlhDC control) also comes to an end, but assembled flagella are active and cells are highly motile. In parallel, the master regulator of the stationary phase, σ, begins to accumulate but initially is only slowly assembling into active RNAP holoenzyme (Eσ). Upon entry into the stationary phase (at an OD of approximately 3), the regulator CsgD is induced, which is essential for the expression of adhesive curli fimbriae and other biofilm-related functions. Note that only relative amounts of the various regulatory proteins or complexes are shown, which cannot be compared directly. OD (578 nm), optical density of the culture measured at 578 nm; ON, overnight, i.e., at approximately 24 h. For further details and references, see the text.

Citation: Hengge R. 2010. Role of Cyclic Di-GMP in the Regulatory Networks of , p 230-252. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch16
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/10.1128/9781555816667.ch16.ch16fig02
Figure 2.
Inverse coordination of motility and curli-mediated adhesion in K-12. The flagellar control cascade (FlhDC/FliA) interferes with the activity of the σ/CsgD/curli control cascade at two levels: (i) FliZ, which is expressed from a class 2 gene in the flagellar hierarchy, is an inhibitor of activity at many -dependent promoters, including those of and and (ii) the PDE YhjH, which is expressed from a class 3 gene (under σ control), degrades c-di-GMP and thereby keeps motility going while not allowing the activation of transcription of and, therefore, curli expression. When the flagellar control cascade (including expression) shuts down in mid-postexponential phase, the DGCs YegE and YedQ, which are increasingly expressed due to the now accumulating , outbalance the PDE activity of YhjH, and c-di-GMP can accumulate. Via YcgR, this c-di-GMP interferes with flagellar activity and, via an unknown effector, stimulates transcription. In essence, this c-di-GMP control module acts as a checkpoint that allows curli expression only after flagellar gene expression has ceased. In parallel, a second DGC/PDE system, YdaM/YciR, is expressed under control. The latter system exclusively acts on transcription in a way which is not additive with the effect of the YegE/YhjH system (but both systems are essential for activation). Additional c-di-GMP control modules operate downstream of CsgD expression and affect the expression of the curli structural operon and cellulose biosynthesis. In principle, the activity of all DGCs and PDEs (probably with the exception of YhjH, which basically consists of an EAL domain only) is likely to be modulated by additional unknown signals (lightning bolts) perceived by their N-terminal sensor domains. Note, only relevant genes or proteins under FlhDC and σ control are shown here; overall, FlhDC and σ activate more than 60 and approximately 500 genes, respectively. For further details and references, see the text. HBB, hook basal body.
10.1128/9781555816667/f0238-01_thmb.gif
10.1128/9781555816667/f0238-01.gif
Image of Figure 2.
Figure 2.

Inverse coordination of motility and curli-mediated adhesion in K-12. The flagellar control cascade (FlhDC/FliA) interferes with the activity of the σ/CsgD/curli control cascade at two levels: (i) FliZ, which is expressed from a class 2 gene in the flagellar hierarchy, is an inhibitor of activity at many -dependent promoters, including those of and and (ii) the PDE YhjH, which is expressed from a class 3 gene (under σ control), degrades c-di-GMP and thereby keeps motility going while not allowing the activation of transcription of and, therefore, curli expression. When the flagellar control cascade (including expression) shuts down in mid-postexponential phase, the DGCs YegE and YedQ, which are increasingly expressed due to the now accumulating , outbalance the PDE activity of YhjH, and c-di-GMP can accumulate. Via YcgR, this c-di-GMP interferes with flagellar activity and, via an unknown effector, stimulates transcription. In essence, this c-di-GMP control module acts as a checkpoint that allows curli expression only after flagellar gene expression has ceased. In parallel, a second DGC/PDE system, YdaM/YciR, is expressed under control. The latter system exclusively acts on transcription in a way which is not additive with the effect of the YegE/YhjH system (but both systems are essential for activation). Additional c-di-GMP control modules operate downstream of CsgD expression and affect the expression of the curli structural operon and cellulose biosynthesis. In principle, the activity of all DGCs and PDEs (probably with the exception of YhjH, which basically consists of an EAL domain only) is likely to be modulated by additional unknown signals (lightning bolts) perceived by their N-terminal sensor domains. Note, only relevant genes or proteins under FlhDC and σ control are shown here; overall, FlhDC and σ activate more than 60 and approximately 500 genes, respectively. For further details and references, see the text. HBB, hook basal body.

Citation: Hengge R. 2010. Role of Cyclic Di-GMP in the Regulatory Networks of , p 230-252. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch16
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/10.1128/9781555816667.ch16.ch16fig03
Figure 3.
The degenerate EAL protein YcgF is a blue light-modulated antirepressor and controls a small-protein and two-component network that modulates biofilm formation. By direct protein-protein interaction, blue light-irradiated YcgF (or excess nonirradiated YcgF) releases the MerR-like repressor YcgE from its operator site upstream of the operon (also and are derepressed, but there the mechanism has not yet been studied). All gene products of these target genes are small proteins (78 to 90 amino acids). YmgB (and YmgA and YcgZ, to minor extents) modulates the biofilm-associated functions indicated via the two-component phosphorelay system RcsC/RcsD/RcsB. The gene also encodes a small protein of unknown molecular function (71 amino acids). In addition, (encoding a small protein of 121 amino acids) is also under control of the YcgF/YcgE/YmgB cascade ( is not included in the figure, as the mechanism of this regulation has not yet been clarified). At the levels of protein activity as well as gene expression, this system integrates blue light, low temperature, starvation, and probably other stress signals and, therefore, seems important for in an extrahost and probably aquatic environment. For further details and references, see the text. Adapted from reference with permission.
10.1128/9781555816667/f0245-01_thmb.gif
10.1128/9781555816667/f0245-01.gif
Image of Figure 3.
Figure 3.

The degenerate EAL protein YcgF is a blue light-modulated antirepressor and controls a small-protein and two-component network that modulates biofilm formation. By direct protein-protein interaction, blue light-irradiated YcgF (or excess nonirradiated YcgF) releases the MerR-like repressor YcgE from its operator site upstream of the operon (also and are derepressed, but there the mechanism has not yet been studied). All gene products of these target genes are small proteins (78 to 90 amino acids). YmgB (and YmgA and YcgZ, to minor extents) modulates the biofilm-associated functions indicated via the two-component phosphorelay system RcsC/RcsD/RcsB. The gene also encodes a small protein of unknown molecular function (71 amino acids). In addition, (encoding a small protein of 121 amino acids) is also under control of the YcgF/YcgE/YmgB cascade ( is not included in the figure, as the mechanism of this regulation has not yet been clarified). At the levels of protein activity as well as gene expression, this system integrates blue light, low temperature, starvation, and probably other stress signals and, therefore, seems important for in an extrahost and probably aquatic environment. For further details and references, see the text. Adapted from reference with permission.

Citation: Hengge R. 2010. Role of Cyclic Di-GMP in the Regulatory Networks of , p 230-252. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch16
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/10.1128/9781555816667.ch16.ch16fig04
Figure 4.
Model for the evolution of second messenger signaling as illustrated by systems operating in The simplest and probably most ancient form of second messenger signaling is represented by the cAMP signaling system (A) ( ). Here, only one second messenger-producing enzyme (the adenylate cyclase Cya), one second messenger-degrading enzyme (the cAMP PDE CpdA), and one effector component (the transcription factor CRP) control a variety of promoter regions that all feature similar cAMP-CRP binding sites. More complex systems that integrate many more signals use multiples of all the components involved, as illustrated by c-di-GMP signaling in the control of flagellar activity and transcription (B). In this system, several DGCs generate c-di-GMP, which in turn serves at least two effector components, indicating that this c-di-GMP is freely diffusible ( ). The multiplicity of DGC, PDEs, effectors, and targets also allows the evolution of locally acting systems, in which complexes consisting of a DGC, a PDE, and an effector highly specifically interact with distinct targets (C). An example seems to be the YdaM/YciR system which specifically regulates transcription ( ) (the tentative protein interactions indicated in the figure are based on unpublished in vivo and in vitro data by S. Lindenberg, H. Weber, and R. Hengge). Finally, the YcgF/YcgE system (which is a paralog of YciR/MlrA) is an example of a locally acting system in which c-di-GMP signaling has been lost and which relies entirely on protein-protein interactions ( ) (D). Adenylate cyclases or DGCs are shown as light gray ovals; PDEs (or proteins derived thereof, such as YcgF) are shown as dark gray hexagons.
10.1128/9781555816667/f0247-01_thmb.gif
10.1128/9781555816667/f0247-01.gif
Image of Figure 4.
Figure 4.

Model for the evolution of second messenger signaling as illustrated by systems operating in The simplest and probably most ancient form of second messenger signaling is represented by the cAMP signaling system (A) ( ). Here, only one second messenger-producing enzyme (the adenylate cyclase Cya), one second messenger-degrading enzyme (the cAMP PDE CpdA), and one effector component (the transcription factor CRP) control a variety of promoter regions that all feature similar cAMP-CRP binding sites. More complex systems that integrate many more signals use multiples of all the components involved, as illustrated by c-di-GMP signaling in the control of flagellar activity and transcription (B). In this system, several DGCs generate c-di-GMP, which in turn serves at least two effector components, indicating that this c-di-GMP is freely diffusible ( ). The multiplicity of DGC, PDEs, effectors, and targets also allows the evolution of locally acting systems, in which complexes consisting of a DGC, a PDE, and an effector highly specifically interact with distinct targets (C). An example seems to be the YdaM/YciR system which specifically regulates transcription ( ) (the tentative protein interactions indicated in the figure are based on unpublished in vivo and in vitro data by S. Lindenberg, H. Weber, and R. Hengge). Finally, the YcgF/YcgE system (which is a paralog of YciR/MlrA) is an example of a locally acting system in which c-di-GMP signaling has been lost and which relies entirely on protein-protein interactions ( ) (D). Adenylate cyclases or DGCs are shown as light gray ovals; PDEs (or proteins derived thereof, such as YcgF) are shown as dark gray hexagons.

Citation: Hengge R. 2010. Role of Cyclic Di-GMP in the Regulatory Networks of , p 230-252. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch16
Permissions and Reprints Request Permissions
Download as Powerpoint

References

/content/book/10.1128/9781555816667.ch16
1. Adler, J., and, B. Templeton. 1967. The effect of environmental conditions on the motility of Escherichia coli. J. Gen. Microbiol. 46: 175– 184.
2. Agladze, K.,, X. Wang, and, T. Romeo. 2005. Spatial periodicity of Escherichia coli K-12 biofilm microstructure initiates during a reversible, polar attachment phase of development and requires the polysaccharide adhesin PGA. J. Bacteriol. 187: 8237– 8246.
3. Amikam, D., and, M. Y. Galperin. 2006. PilZ domain is part of the bacterial c-di-GMP binding protein. Bioinformatics 22: 3– 6.
4. Amsler, C. D.,, M. Cho, and, P. Matsumura. 1993. Multiple factors underlying the maximum motility of Escherichia coli as cultures enter post-exponential growth. J. Bacteriol. 175: 6238– 6244.
5. Baker, D. A., and, J. M. Kelly. 2004. Structure, function and evolution of microbial adenylyl and guanylyl cyclases. Mol. Microbiol. 52: 1229– 1242.
6. Barembruch, C., and, R. Hengge. 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.
7. Beloin, C.,, A. Roux, and, J.-M. Ghigo. 2008. Escherichia coli biofilms. Curr. Top. Microbiol. Immunol. 322: 249– 289.
8. Boehm, A.,, S. Steiner,, F. Zaehringer,, A. Casanova,, F. Hamburger,, D. Ritz,, W. Keck,, M. Ackerman,, T. Schirmer, and, U. Jenal. 2009. Second messenger signaling governs Escherichia coli biofilm induction upon ribosomal stress. Mol. Microbiol. 72: 1500– 1516.
9. Botsford, J. L., and, J. G. Harman. 1992. Cyclic AMP in prokaryotes. Microbiol. Rev. 56: 100– 122.
10. Bougdour, A.,, C. Lelong, and, J. Geiselmann. 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.
11. Branda, S. S.,, A. Vik,, L. Friedman, and, R. Kolter. 2005. Biofilms: the matrix revisited. Trends Microbiol. 13: 20– 26.
12. Brombacher, E.,, A. Baratto,, C. Dorel, and, P. Landini. 2006. Gene expression regulation by the curli activtor CsgD protein: modulation of cellulose biosynthesis and control of negative determinants for microbial adhesion. J. Bacteriol. 188: 2027– 2037.
13. Brombacher, E.,, C. Dorel,, A. J. B. 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: 2847– 2857.
14. Brown, N. L.,, J. V. Stoyanov,, S. P. Kidd, and, J. L. Hobman. 2003. The MerR family of transcriptional regulators. FEMS Microbiol. Rev. 27: 145– 163.
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: 349– 363.
16. Cairrao, F.,, A. Chora,, R. Zilhao,, A. J. Carpousis, and, C. M. Arraiano. 2001. RNase II levels change according to the growth conditions: characterization of gmr, a new Escherichia coli gene involved in the modulation of RNase II. Mol. Microbiol. 39: 1550– 1561.
17. Cerca, N.,, T. Maira-Litrán,, K. K. Jefferson,, M. Grout,, D. A. Goldmann, and, G. B. Pier. 2007. Protection against Escherichia coli infection by antibody to the Staphylococcus aureus poly-N-acetylglucosamine surface polysaccharide. Proc. Natl. Acad. Sci. USA 104: 7528– 7533.
18. Chan, C.,, R. Paul,, D. Samoray,, N. Amiot,, B. Giese,, U. Jenal, and, T. Schirmer. 2004. Structural basis of activity and allosteric control of diguanylate cyclase. Proc. Natl. Acad. Sci. USA 101: 17084– 17089.
19. Chang, A. L.,, J. R. Tuckerman,, G. Gonzalez,, R. Mayer,, H. Weinhouse,, G. Volman,, D. Amikam,, M. Benziman, and, M.-A. Gilles-Gonzalez. 2001. Phosphodiesterase A1, a regulator of cellulose synthesis in Acetobacter xylinum, is a heme-based sensor. Biochemistry 40: 3420– 3426.
20. Chevance, F. F. V., and, K. T. Hughes. 2008. Coordinating assembly of a bacterial macromolecular machine. Nat. Rev. Microbiol. 6: 455– 465.
21. Chilcott, G. S., and, K. T. Hughes. 2000. Coupling of flagellar gene expression to flagellar assembly in Salmonella enterica serovar Typhimurium and Escherichia coli. Microbiol. Mol. Biol. Rev. 64: 694– 708.
22. Christen, B.,, M. Christen,, R. Paul,, F. Schmid,, M. Folcher,, P. Jenoe,, M. Meuwly, and, U. Jenal. 2006. Allosteric control of cyclic di-GMP signaling. J. Biol. Chem. 281: 32015– 32024.
23. Christen, M.,, B. Christen,, M. G. Allan,, M. Folcher,, P. Jenö,, S. Grzesiek, and, U. Jenal. 2007. DgrA is a member of a new family of cyclic diguanosine monophosphate receptors and controls flagellar motor function in Caulobacter crescentus. Proc. Natl. Acad. Sci. USA 104: 4112– 4117.
24. 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: 30829– 30837.
25. Claret, L.,, S. Miquel,, N. Vieille,, D. A. Ryjenkov,, L. Gomelsky, and, A. Darfeuille-Michaud. 2007. The flagellar sigma factor FliA regulates adhesion and invasion of Crohn disease-associated Escherichia coli via a cyclic dimeric GMP-de-pendent pathway. J. Biol. Chem. 282: 33275– 33283.
26. Costanzo, A., and, S. Ades. 2006. Growth phase-dependent regulation of the extracytoplasmic stress factor, sigmaE by guanosine 3′,5′-bispyrophosphate (ppGpp). J. Bacteriol. 188: 4627– 4634.
27. Danese, P.,, L. A. Pratt, and, R. Kolter. 2000. Exopolysacchar-ide production is required for development of Escherichia coli K-12 biofilm architecture. J. Bacteriol. 182: 3593– 3596.
28. De, N.,, M. Pirruccello,, P. V. Krasteva,, N. Bae,, R. V. Raghavan, and, H. Sondermann. 2008. Phosphorylation-independent regulation of the diguanylate cyclase WspR. PLoS Biol. 6: e67.
29. Delgado-Nixon,, V. M.,, G. Gonzalez, and, M.-A. Gilles-Gonzalez. 2000. Dos, a heme-binding PAS protein from Escherichia coli, is a direct oxygen sensor. Biochemistry 39: 2685– 2691.
30. Domka, J.,, J. Lee,, T. Bansal, and, T. K. Wood. 2007. Temporal gene expression in Escherichia coli K-12 biofilms. Environ. Microbiol. 9: 332– 346.
31. Duerig, A.,, M. Folcher,, S. Abel,, M. Nicollier,, T. Schwede,, N. Amiot,, B. Giese, and, U. Jenal. 2009. Second messenger-mediated spatiotemporal control of protein degradation regulates bacterial cell cycle progression. Genes Dev. 23: 93– 104.
32. Eguchi, Y.,, J. Itou,, M. Yamane,, R. Demizu,, F. Yamato,, A. Okada,, H. Mori,, A. Kato, and, R. Utsumi. 2007. B1500, a small membrane protein, connects the two-component systems EvgS/EvgA and PhoQ/PhoP in Escherichia coli. Proc. Natl. Acad. Sci. USA 104: 18712– 18717.
33. Frye, J.,, J. E. Karlinsey,, H. R. Felise,, B. Marzolf,, N. Dowidar,, M. McClelland, and, K. T. Hughes. 2006. Identification of new flagellar genes of Salmonella enterica serovar Typhimurium. J. Bacteriol. 188: 2233– 2243.
34. Galperin, M. Y. 2004. Bacterial signal transduction network in a genomic perspective. Environ. Microbiol. 6: 552– 567.
35. Galperin, M. Y. 2005. A census of membrane-bound and intracellular signal transduction proteins in bacteria: bacterial IQ, extroverts and introverts. BMC Microbiol. 5: 35.
36. 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: 11– 21.
37. Gentry, D. R.,, V. J. Hernandez,, L. H. Nguyen,, D. B. Jensen, and, M. Cashel. 1993. Synthesis of the stationary-phase sigma factor σ S is positively regulated by ppGpp. J. Bacteriol. 175: 7982– 7989.
38. Girgis, H. S.,, Y. Liu,, W. S. Ryu, and, S. Tavazoie. 2007. A comprehensive genetic characterization of bacterial motility. PLoS Genetics 3: e154.
39. Goller, C., and, T. Romeo. 2008. Environmental influences on biofilm development. Curr. Top. Microbiol. Immunol. 322: 37– 66.
40. Goller, C.,, X. Wang,, Y. Itoh, and, T. Romeo. 2006. The cation-responsive protein NhaR of Escherichia coli activates pgaABCD transcription, required for production of the biofilm adhesin poly-beta-1,6- N-acetyl-D-glucosamine. J. Bacteriol. 188: 8022– 8032.
41. Gomelsky, M., and, G. Klug. 2002. BLUF: a novel FAD-binding domain involved in sensory transduction in microorganisms. Trends Biochem. Sci. 27: 497– 500.
42. Grigorova, I. R.,, N. J. Phleger,, V. K. Mutalik, and, C. A. Gross. 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.
43. Gruber, T., and, C. A. Gross. 2003. Multiple sigma subunits and the partitioning of bacterial transcription space. Annu. Rev. Microbiol. 57: 441– 466.
44. Hammar, M.,, A. Arnquist,, Z. Bian,, A. Olsen, and, S. Normark. 1995. Expression of two csg operons is required for production of fibronectin- and Congo red-binding curli polymers in Escherichia coli K-12. Mol. Microbiol. 18: 661– 670.
45. Hanna, A.,, M. Berg,, V. Stout, and, A. Razatos. 2003. Role of capsular colanic acid in adhesion of uropathogenic Escherichia coli. Appl. Environ. Microbiol. 69: 4474– 4481.
46. Hasegawa, K.,, S. Masuda, and, T. A. Ono. 2006. Light induced structural changes of a full-length protein and its BLUF domain in YcgF (Blrp), a blue-light sensing protein that uses FAD (BLUF). Biochemistry 45: 3785– 3793.
47. Hengge, R. 2009. Principles of cyclic-di-GMP signaling. Nat. Rev. Microbiol. 7: 263– 273.
48. Hengge-Aronis,, R. 2000. The general stress response in Escherichia coli, p. 161–178. In G. Storz and, R. Hengge-Aronis (ed.), Bacterial Stress Responses. ASM Press, Washington, DC.
49. Hickman, J. W., and, C. S. Harwood. 2008. Identification of FleQ from Pseudomonas aeruginosa as a c-di-GMP-responsive transcription factor. Mol. Microbiol. 69: 376– 389.
50. Holland, K.,, S. J. Busby, and, G. S. Lloyd. 2007. New targets for the cyclic AMP receptor protein in the Escherichia coli K-12 genome. FEMS Microbiol. Lett. 274: 89– 94.
51. Hurley, J. H. 2003. GAF domains: cyclic nucleotides come full circle. Sci. STKE 164: pe1.
52. Itoh, Y.,, J. D. Rice,, C. Goller,, A. Pannuri,, J. Taylor,, J. Meisner,, T. J. Beveridge,, J. F. Preston III, and, T. Romeo. 2008. Roles of pgaABCD genes in synthesis, modification, and export of the Escherichia coli biofilm adhesin poly-β-1,6-N-acetyl-D-glucosamine. J. Bacteriol. 190: 3670– 3680.
53. Jenal, U., and, J. Malone. 2006. Mechanisms of cyclic-di-GMP signaling in bacteria. Annu. Rev. Genet. 40: 385– 407.
54. Jin, D. J., and, J. E. Cabrera. 2006. Coupling the distribution of RNA polymerase to global gene regulation and the dynamic structure of the bacterial nucleoid in Escherichia coli. J. Struct. Biol. 156: 284– 291.
55. Jishage, M., and, A. Ishihama. 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.
56. Jishage, M., and, A. Ishihama. 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.
57. Jishage, M.,, K. Kvint,, V. Shingler, and, T. Nystróm. 2002. Regulation of sigma factor competition by the alarmone ppGpp. Genes Dev. 16: 1260– 1270.
58. Jonas, K.,, A. N. Edwards,, R. Simm,, T. Romeo,, U. Römling, and, O. Melefors. 2008. The RNA binding protein CsrA controls c-di-GMP metabolism by directly regulating the expression of GGDEF proteins. Mol. Microbiol. 70: 236– 257.
59. Jonas, K.,, H. Tomenius,, A. Kader,, S. Normark,, U. Römling,, L. B. Belova, and, O. Melefors. 2007. Roles of curli, cellulose and BapA in Salmonella biofilm morphology studied by atomic force microscopy. BMC Microbiol. 7: 70.
60. 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: 2038– 2049.
61. 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: 602– 616.
62. Kalir, S., and, U. Alon. 2004. Using a quantitative blueprint to reprogram the dynamics of the flagella gene network. Cell 117: 713– 720.
63. Kaper, J. B.,, J. P. Nataro, and, H. L. T. Mobley. 2004. Pathogenic Escherichia coli. Nat. Rev. Microbiol. 2: 123– 140.
64. Kato, A., and, E. A. Groisman. 2004. Connecting two-component regulatory systems by a protein that protects a response regulator from dephosphorylation by its cognate sensor. Genes Dev. 18: 2302– 2313.
65. Kato, A.,, A. Y. Mitrophanov, and, E. A. Groisman. 2007. A connector of two-component regulatory systems promotes signal amplification and persistence of expression. Proc. Natl. Acad. Sci. USA 104: 12063– 12068.
66. Klausen, M.,, M. Gjermansen,, J. U. Kreft, and, T. Tolker-Nielsen. 2006. Dynamics of development and dispersal in sessile microbial communities: examples from Pseudomonas aeruginosa and Pseudomonas putida model biofilms. FEMS Microbiol. Lett. 261: 1– 11.
67. 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: 371– 382.
68. Lacour, S., and, P. Landini. 2004. σ S-dependent gene expression at the onset of stationary phase in Escherichia coli: function of σ S-dependent genes and identification of their promoter sequences. J. Bacteriol. 186: 7186– 7195.
69. Lane, M. C.,, A. N. Simms, and, H. L. Mobley. 2007. Complex interplay between type 1 fimbrial expression and flagellum-mediated motility of uropathogenic Escherichia coli. J. Bacteriol. 189: 5523– 5533.
70. Lange, R.,, D. Fischer, and, R. Hengge-Aronis. 1995. Identification of transcriptional start sites and the role of ppGpp in the expression of rpoS, the structural gene for the σ S subunit of RNA-polymerase in Escherichia coli. J. Bacteriol. 177: 4676– 4680.
71. Lange, R., and, R. Hengge-Aronis. 1994. The cellular concentration of the σ S subunit of RNA-polymerase in Escherichia coli is controlled at the levels of transcription, translation and protein stability. Genes Dev. 8: 1600– 1612.
72. Lange, R., and, R. Hengge-Aronis. 1991. Growth phase-regulated expression of bolA and morphology of stationary phase Escherichia coli cells is controlled by the novel sigma factor σ S ( rpoS). J. Bacteriol. 173: 4474– 4481.
73. Lange, R., and, R. Hengge-Aronis. 1991. Identification of a central regulator of stationary-phase gene expression in Escherichia coli. Mol. Microbiol. 5: 49– 59.
74. Lee, J.,, A. Jayaraman, and, T. K. Wood. 2007. Indole is an inter-species biofilm signal mediated by SdiA. BMC Microbiol. 7: 42.
75. Lee, J.,, R. Page,, R. Garcla-Contreras,, J.-M., Palermino,, X.-S., Zhang,, O. Doshi,, T. K. Wood, and, W. Peti. 2007. Structure and function of the Escherichia coli protein YmgB: a protein critical for biofilm formation and acid resistance. J. Mol. Biol. 373: 11– 26.
76. Lin, Z.,, L. C. Johnson,, H. Weissbach,, N. Brot,, M. O. Livel, and, W. T. Lowther. 2007. Free methionine-(R)-sulfoxide re-ductase from Escherichia coli reveals a new GAF domain function. Proc. Natl. Acad. Sci. USA 104: 9597– 9602.
77. Maeda, H.,, N. Fujita, and, A. Ishihama. 2000. Competition among seven Escherichia coli sigma subunits: relative binding affinities to the core RNA polymerase. Nucleic Acids Res. 28: 3497– 3503.
78. Majdalani, N., and, S. Gottesman. 2005. The Rcs phospho-relay: a complex signal transduction system. Annu. Rev. Microbiol. 599: 379– 405.
79. McCann, M. P.,, J. P. Kidwell, and, A. Matin. 1991. The putative sigma factor KatF has a central role in development of starvation-mediated general resistance in Escherichia coli. J. Bacteriol. 173: 4188– 4194.
80. Méndez-Ortiz,, M. M.,, M. Hyodo,, Y. Hayakawa, and, J. Membrillo-Hernández. 2006. Genome wide transcription profile of Escherichia coli in response to high levels of the second messenger c-diGMP. J. Biol. Chem. 281: 8090– 8099.
81. Merighi, M.,, V. T. Lee,, M. Hyodo,, Y. Hayakawa, and, S. Lory. 2007. The second messenger bis-(3′-5′)-cyclic-GMP and its PilZ domain-containing receptor Alg44 are required for alginate biosynthesis in Pseudomonas aeruginosa. Mol. Microbiol. 65: 876– 895.
82. Minasov, G.,, S. Padavattan,, L. Shuvalova,, J. S. Brunzelle,, D. J. Miller,, A. Basláe,, 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: 13174– 13184.
83. Nakasone, Y.,, T. A. Ono,, A. Ishii,, S. Masuda, and, M. Terazima. 2007. Transient dimerization and conformational change of a BLUF protein: YcgF. J. Am. Chem. Soc. 129: 7028– 7035.
84. Newell, P. D.,, R. D. Monds, and, G. A. O’Toole. 2009. LapD is a bis-(3′,5′)-cyclic dimeric GMP-binding protein that regulates surface attachment by Pseudomonas fluorescens Pf0-1. Proc. Natl. Acad. Sci. USA 106: 3461– 3466.
85. Nikolskaya, A. N.,, A. Y. Mulkidjanian,, I. B. Beech, and, M. Y. Galperin. 2003. MASE1 and MASE2: two novel integral membrane sensory domains. J. Mol. Microbiol. Biotechnol. 5: 11– 16.
86. Oglesby, L.,, S. Jain, and, D. E. Ohman. 2008. Membrane topology and roles of Pseudomonas aeruginosa Alg8 and Alg44 in alginate polymerization. Microbiology 154: 1605– 1615.
87. Olsén, A.,, A. Jonsson, and, S. Normark. 1989. Fibronectin binding mediated by a novel class of surface organelles on Escherichia coli. Nature 338: 652– 655.
88. Partridge, J. D.,, G. Sanguinetti,, D. P. Dibden,, R. E. Roberts,, R. K. Poole, and, J. Green. 2007. Transition of Escherichia coli from aerobic to micro-aerobic conditions involves fast and slow reacting regulatory components. J. Biol. Chem. 282: 11230– 11237.
89. Patten, C. L.,, M. G. Kirchhhof,, M. R. Schertzberg,, R. A. Morton, and, H. E. Schellhorn. 2004. Microarray analysis of RpoS-mediated gene expression in Escherichia coli K-12. Mol. Genet. Genomics 272: 580– 591.
90. Paul, R.,, S. Weiser,, N. 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: 715– 727.
91. 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: 2434– 2446.
92. Pesavento, C., and, R. Hengge. 2009. Bacterial nucleotide-based second messengers. Curr. Opin. Microbiol. 12: 170– 176.
93. Peters, J. E.,, T. E. Thate, and, N. L. Craig. 2003. Definition of the Escherichia coli MC4100 genome by use of a DNA array. J. Bacteriol. 185: 2017– 2021.
94. Potrykus, K., and, M. Cashel. 2008. (p)ppGpp: still magical? Annu. Rev. Microbiol. 62: 35– 51.
95. Pratt, L. A., and, R. Kolter. 1999. Genetic analyses of bacterial biofilm formation. Curr. Opin. Microbiol. 2: 598– 603.
96. Pratt, L. A., and, T. J. Silhavy. 1998. Crl stimulates RpoS activity during stationary phase. Mol. Microbiol. 29: 1225– 1236.
97. Prigent-Combaret,, C.,, E. Brombacher,, O. Vidal,, A. Ambert,, P. Lejeune,, P. Landini, and, C. Dorel. 2001. Complex regulatory network controls initial adhesion and biofilm formation in Escherichia coli via regulation of the csgD gene. J. Bacteriol. 183: 7213– 7223.
98. Prigent-Combaret,, C.,, G. Prensier,, T. T. Le Thi,, Q. Vidal,, P. Lejeune, and, C. Dorel. 2000. Developmental pathway for biofilm formation in curli-producing Escherichia coli strains: role of flagella, curli and colanic acid. Environ. Microbiol. 2: 450– 464.
99. Prigent-Combaret,, C.,, O. Vidal,, C. Dorel, and, P. Lejeune. 1999. Abiotic surface sensing and biofilm-dependent regulation of gene expression in Escherichia coli. J. Bacteriol. 181: 5993– 6002.
100. Prüβ, B. M.,, C. Besemann,, A. Denton, and, A. J. Wolfe. 2006. A complex transcription network controls the early stages of biofilm development in Escherichia coli. J. Bacteriol. 188: 3731– 3739.
101. Rajagopal, S.,, J. M. Key,, E. B. Purcell,, D. J. Boerema, and, K. Moffat. 2004. Purification and initial characterization of a putative blue light-regulated phosphodiesterase from Escherichia coli. Photochem. Photobiol. 80: 542– 547.
102. Rao, F.,, Y. Yang,, Y. Qi, and, Z. X. Liang. 2008. Catalytic mechanism of c-di-GMP specific phosphodiesterase: a study of the EAL domain-containing RocR from Pseudomonas aeruginosa. J. Bacteriol. 190: 3622– 3631.
103. Regonesi, M. E.,, M. Del Favero,, F. Basilico,, F. Briani,, L. Benazzi,, P. Tortora,, P. Mauri, and, G. Dehó. 2006. Analysis of the Escherichia coli RNA degradosome composition by a proteomic approach. Biochimie 88: 151– 161.
104. Römling, 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: 722– 731.
105. Römling, U.,, M. Gomelsky, and, M. Y. Galperin. 2005. C-di-GMP: the dawning of a novel bacterial signalling system. Mol. Microbiol. 57: 629– 639.
106. Römling, U.,, M. Rohde,, A. Olsáen,, S. Normark, and, J. Reinkoóster. 2000. AgfD, the checkpoint of multicellular and aggregative behaviour in Salmonella typhimurium regulates at least two independent pathways. Mol. Microbiol. 36: 10– 23.
107. Römling, U.,, W. D. Sierralta,, K. Eriksson, and, S. Normark. 1998. Multicellular and aggregative behaviour of Salmonella typhimurum strains is controlled by mutations in the agfD promoter. Mol. Microbiol. 28: 249– 264.
108. Ross, P.,, H. Weinhouse,, Y. Aloni,, D. Michaeli,, P. Weinberger-Ohana,, R. Mayer,, S. Braun,, E. de Vroom,, G. A. van der Marel,, J. H. van Boom, and, M. Benziman. 1987. Regulation of cellulose synthesis in Acetobacter xylinum by cyclic diguanylate. Nature 325: 279– 281.
109. Ryan, R. P.,, Y. Fouhy,, F. Lucey, and, J. M. Dow. 2006. Cyclic di-GMP signaling in bacteria: recent advances and new puzzles. J. Bacteriol. 188: 8327– 8334.
110. Ryan, R. P.,, Y. Fouhy,, J. F. Lucey,, L. C. Crossman,, S. Spiro,, Y.-W., He,, L.-H., Zhang,, S. Heeb,, P. Williams, and, J. M. Dow. 2006. Cell-cell signaling in Xanthomonas campestris involves an HD-GYP domain protein that functions in cyclic di-GMP turnover. Proc. Natl. Acad. Sci. USA 103: 6712– 6717.
111. Rychlik, I.,, G. Martin,, U. Methner,, M. Lovell,, L. Cardova,, A. Sebkova,, M. Sevcik,, J. Damborsky, and, P. A. Barrow. 2002. Identification of Salmonella enterica serovar Typhimurium genes associated with growth suppression in stationary-phase nutrient broth cultures and in the chicken intestine. Arch. Microbiol. 178: 411– 420.
112. Ryjenkov, D. A.,, R. Simm,, U. Römling, and, M. Gomelsky. 2006. The PilZ domain is a receptor for the second messenger c-di-GMP: the PilZ protein YcgR controls motility in enterobacteria. J. Biol. Chem. 281: 30310– 30314.
113. Ryjenkov, D. A.,, M. Tarutina,, O. V. Moskvin, and M. Go-melsky. 2005. Cyclic diguanylate is a ubiquitous signaling molecule in bacteria: insights into biochemistry of the GGDEF protein domain. J. Bacteriol. 187: 1792– 1798.
114. 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: 4774– 4781.
115. Schroeder, C.,, K. Werner,, H. Otten,, S. Króatzig,, H. Schwalbe, and, L.-O. Essen. 2008. Influence of a joining helix on the BLUF domain of the YcgF photoreceptor from Escherichia coli. Chembiochem 9: 2463– 2473.
116. Sezonov, G.,, D. Joseleau-Petit, and, R. D’Ari. 2007. Escherichia coli physiology in Luria-Bertani broth. J. Bacteriol. 189: 8746– 8749.
117. Shenoy, A. R.,, K. Sivakumar,, A. Krupa,, N. Srinivasan, and, S. S. Visweswariah. 2004. A survey of nucleotide cyclases in actinobacteria: unique domain organisation and expansion of the class III cyclase family in Mycobacterium tuberculosis. Comp. Funct. Genomics 5: 17– 38.
118. Shenoy, A. R., and, S. S. Visweswariah. 2004. Class III nucleotide cyclases in bacteria and archaebacteria: lineage-specific expansion of adenylyl cyclases and a dearth of guanylyl cyclases. FEBS Lett. 561: 11– 21.
119. Shenoy, A. R., and, S. S. Visweswariah. 2006. New messages from old messengers: cAMP and mycobacteria. Trends Microbiol. 14: 543– 550.
120. Simm, R.,, A. Lusch,, A. Kader,, M. Andersson, and, U. Römling. 2007. Role of EAL-containing proteins in multicellular behavior of Salmonella enterica serovar Typhimurium. J. Bacteriol. 189: 3613– 3623.
121. Sommerfeldt, N.,, A. Possling,, G. Becker,, C. Pesavento,, N. Tschowri, and, R. Hengge. 2009. Gene expression patterns and differential input into curli fimbriae regulation of all GGDEF/EAL domain proteins in Escherichia coli. Microbiology 155: 1318– 1331.
122. Soutourina, O.,, A. Kolb,, E. Krin,, C. Laurent-Winter,, S. Rimsky,, A. Danchin, and, P. Bertin. 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.
123. Storz, G., and, R. Hengge-Aronis (ed.). 2000. Bacterial Stress Responses. ASM Press, Washington, DC.
124. Sudarsan, N.,, E. R. Lee,, Z. Weinberg,, R. H. Moy,, J. N. Kim,, K. H. Link, and, R. R. Breaker. 2008. Riboswitches in eubacteria sense the second messenger cyclic di-GMP. Science 321: 411– 413.
125. 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: 2605– 2617.
126. 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: 4416– 4425.
127. Tamayo, R.,, A. D. Tischler, and, A. Camilli. 2005. The EAL domain protein VieA is a cyclic diguanylate phosphodiesterase. J. Biol. Chem. 280: 33324– 33330.
128. Taylor, B. L., and, I. G. Zhulin. 1999. PAS domains: internal sensors of oxygen, redox potential, and light. Microbiol. Mol.Biol. Rev. 63: 479– 506.
129. Tomoyasu, T.,, A. Takaya,, E. Isogai, and, T. Yamamoto. 2003. Turnover of FlhD and FlhC, master regulator proteins for Salmonella flagellum biogenesis, by the ATP-dependent ClpXP protease. Mol. Microbiol. 48: 443– 452.
130. Tschowri, N.,, S. Busse, and, R. Hengge. 2009. The BLUF-EAL protein YcgF acts as a direct anti-repressor in a blue light response of E. coli. Genes Dev. 23: 522– 534.
131. Typas, A.,, C. Barembruch, and, R. Hengge. 2007. Stationary phase reorganisation of the E. coli transcription machinery by Crl protein, a fine-tuner of σ S activity and levels. EMBO J. 26: 1569– 1578.
132. Vianney, A.,, G. Jubelin,, S. Renault,, C. Dorel,, P. Lejeune, and, J. C. Lazzaroni. 2005. Escherichia coli tol and rcs genes participate in the complex network affecting curli synthesis. Microbiology 151: 2487– 2497.
133. Vidal, O.,, R. Longin,, C. Prigent-Combaret,, C. Dorel,, M. Heooreman, and, P. Lejeune. 1998. Isolation of an Escherichia coli K-12 mutant strain able to form biofilms on inert surfaces: involvement of a new ompR allele that increases curli expression. J. Bacteriol. 180: 2442– 2449.
134. Wan, X.,, J. R. Tuckerman,, J. A. Saito,, T. A. K. Freitas,, J. S. Newhouse,, J. R. Denery,, M. Y. Galperin,, G. Gonzalez,, M.-A. Gilles-Gonzalez, and, M. Alam. 2009. Globins synthesize the second messenger bis-(3′-5′)-cyclic diguanosine monophosphate in bacteria. J. Mol. Biol. 388: 262– 270.
135. 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: 1648– 1663.
136. Wassmann, P.,, C. Chan,, R. Paul,, A. Beck,, H. Heerklotz,, U. Jenal, and, T. Schirmer. 2007. Structure of BeF3-modified response regulator PleD: implications of diguanylate cyclase activation, catalysis, and feedback inhibition. Structure (Cambridge) 15: 915– 927.
137. Weber, H.,, C. Pesavento,, A. Possling,, G. Tischendorf, and, R. Hengge. 2006. Cyclic-di-GMP-mediated signaling within the σ S network of Escherichia coli. Mol. Microbiol. 62: 1014– 1034.
138. Weber, H.,, T. Polen,, J. Heuveling,, V. Wendisch, and, R. Hengge. 2005. Genome-wide analysis of the general stress response network in Escherichia coli: σ S-dependent genes, promoters and sigma factor selectivity. J. Bacteriol. 187: 1591– 1603.
139. Weinhouse, H.,, S. Sapir,, D. Amikam,, Y. Shilo,, G. Volman,, P. Ohana, and, M. Benziman. 1997. c-di-GMP-binding protein, a new factor regulating cellulose synthesis in Acetobacter xylinum. FEBS Lett. 416: 207– 211.
140. Willoughby, D., and, D. M. Cooper. 2007. Organization and Ca 2+ regulation of adenylyl cyclases in cAMP microdomains. Physiol. Rev. 87: 965– 1010.
141. 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: 463– 475.
142. Wood, T. K.,, A. F. Gonzáalez-Barrios,, M. Herzberg, and, J. Lee. 2006. Motility influences biofilm architecture in Escherichia coli. Appl. Environ. Microbiol. 72: 361– 367.
143. Wozniak, C. E.,, C. Lee, and, K. T. Hughes. 2009. T-POP array identifies EcnR and PefI-SrgD as novel regulators of flagellar gene expression. J. Bacteriol. 191: 1498– 1508.
144. Wu, Q., and, K. Gardner. 3 February 2009. Structure and insight into the blue light-induced changes in the BirP1 BLUF domain. Biochemistry 48: 2620– 2629.
145. Yamamoto, K., and, A. Ishihama. 2006. Characterization of copper-inducible promoters regulated by CpxA/CpxR in Escherichia coli. Biosci. Biotechnol. Biochem. 70: 1688– 1695.
146. Zhao, K.,, M. Liu, and, R. R. Burgess. 2007. Adaptation in bacterial flagellar and motility systems: from regulon members to “foraging”-like behavior in E. coli. Nucleic Acids Res. 35: 4441– 4452.
147. Zhou, X.,, X. Meng, and, B. Sun. 2008. An EAL domain protein and cyclic AMP contribute to the interaction between the two quorum sensing systems in Escherichia coli. Cell Res. 18: 937– 948.
148. 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: 1452– 1463.
149. Zoraghi, R.,, J. D. Corbin, and, S. H. Francis. 2004. Properties and functions of GAF domain in cyclic nucleotide phosphodiesterases and other proteins. Mol. Pharmacol. 65: 267– 278.

Tables

Role of Cyclic Di-GMP in the Regulatory Networks of Escherichia coli
[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555816667.ch16-1,webId=/content/author/10.1128/9781555816667.ch16-1,properties={foaf_givenname=Regine, foaf_name=Regine Hengge, foaf_surname=Hengge, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555816667.ch16-aff1]]}]]
Citation: Hengge R. 2010. Role of Cyclic Di-GMP in the Regulatory Networks of , p 230-252. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch16
/content/10.1128/9781555816667.ch16.ch16tab01
Table 1
GGDEF/EAL genes in and serovar Typhimurium
Generic image for table
Table 1

GGDEF/EAL genes in and serovar Typhimurium

Citation: Hengge R. 2010. Role of Cyclic Di-GMP in the Regulatory Networks of , p 230-252. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch16
/content/10.1128/9781555816667.ch16.ch16tab02
Table 2
Summary of sequence features and expression data of GGDEF/EAL genes in K-12
Generic image for table
Table 2

Summary of sequence features and expression data of GGDEF/EAL genes in K-12

Citation: Hengge R. 2010. Role of Cyclic Di-GMP in the Regulatory Networks of , p 230-252. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch16

Back to top
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