The EAL domain protein YciR acts as a trigger enzyme in a c-di-GMP signalling cascade in E. coli biofilm control

EMBO Journal

Volumn 32, Issue 14, 2013, Pages 2001-2014

  Lindenberg, Sandra ^a   Klauck, Gisela ^a   Pesavento, Christina ^a,b   Klauck, Eberhard ^a   Hengge, Regine ^a  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

Amyloid; CsgD; Curli fibres; Cyclic di GMP; GGDEF domain

Indexed keywords

EAL PROTEIN; GUANOSINE PHOSPHATE; MERR PROTEIN; PHOSPHODIESTERASE; UNCLASSIFIED DRUG; YCIR PROTEIN;

ARTICLE; BIOFILM; CONTROLLED STUDY; ENZYME ACTIVITY; ESCHERICHIA COLI; GENETIC ANALYSIS; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; SIGNAL TRANSDUCTION;

BIOFILMS; CYCLIC GMP; ESCHERICHIA COLI K12; ESCHERICHIA COLI PROTEINS; MODELS, BIOLOGICAL; MULTIPROTEIN COMPLEXES; PHOSPHORUS-OXYGEN LYASES; PROTEIN INTERACTION DOMAINS AND MOTIFS; SECOND MESSENGER SYSTEMS; SIGNAL TRANSDUCTION; TRANS-ACTIVATORS; TRANSCRIPTION, GENETIC;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 84880331924     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2013.120     Document Type: Article

References (60)

1. Abel S, Chien P, Wassmann P, Schirmer T, Kaever V, Laub MT, Baker TA, Jenal U (2011) Regulatory cohesion of cell cycle and cell differentiation through interlinked phosphorylation and second messenger networks. Mol Cell 43: 550-560
2. Alén C, Sonenshein AL (1999) Bacillus subtilis aconitase is an RNA-binding protein. Proc Natl Acad Sci USA 96: 10412-10417 (Pubitemid 29422572)
3. Amikam D, Galperin MY (2006) PilZ domain is part of the bacterial c-di-GMP binding protein. Bioinformatics 22: 3-6 (Pubitemid 43057001)
4. Andrade MO, Alegria MC, Guzzo CR, Docena C, Rosa MC, Ramos CH, Farah CS (2006) The HD-GYP domain of RpfG mediates a direct linkage between the Rpf quorum-sensing pathway and a subset of diguanylate cyclase proteins in the phytopathogen Xanthomonas axonopodis pv citri. Mol Microbiol 62: 537-551 (Pubitemid 44477240)
5. Becker G, Klauck E, Hengge-Aronis R (1999) Regulation of RpoS proteolysis in Escherichia coli: The response regulator RssB is a recognition factor that interacts with the turnover element in RpoS. Proc Natl Acad Sci USA 96: 6439-6444 (Pubitemid 29256684)
6. Bobrov AG, Kirillina O, Forman S, Mack D, Perry RD (2008) Insights into Yersinia pestis biofilm development: Topology and co-interaction of Hms inner membrane proteins involved in exopolysaccharide production. Environ Microbiol 10: 1419-1432 (Pubitemid 351670241)
7. Boehm A, Kaiser M, Li H, Spangler C, Kasper CA, Ackerman M, Kaever V, Sourjik V, Roth V, Jenal U (2010) Second messengermediated adjustment of bacterial swimming velocity. Cell 141: 107-116
8. Brown NL, Stoyanov JV, Kidd SP, Hobman JL (2003) The MerR family of transcriptional regulators. FEMS Microbiol Rev 27: 145-163 (Pubitemid 36694653)
9. Brown PK, Dozois CM, Nickerson CA, Zuppardo A, Terlonge J, Curtiss III R (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 (Pubitemid 32730536)
10. Chan C, Paul R, Samoray D, Amiot N, Giese B, Jenal U, Schirmer T (2004) Structural basis of activity and allosteric control of diguanylate cyclase. Proc Natl Acad Sci USA 101: 17084-17089 (Pubitemid 39627778)
11. Chin KH, Lee YC, Tu ZL, Chen CH, Tseng YH, Yang JM, Ryan RP, McCarthy Y, Dow JM, Wang AH, Chou SH (2009) The cAMP receptor-like protein CLP is a novel c-di-GMP receptor linking cell-cell signaling to virulence gene expression in Xanthomonas campestris. J Mol Biol 396: 646-662
12. Christen B, Christen M, Paul R, Schmid F, Folcher M, Jenoe P, Meuwly M, Jenal U (2006) Allosteric control of cyclic di-GMP signaling. J Biol Chem 281: 32015-32024 (Pubitemid 46041462)
13. Christen B, Kulasakara HD, Christen B, Kulasakara BR, Hoffmann LR, Miller SI (2010) Asymmetrical distribution of the second messenger c-di-GMP upon bacterial cell division. Science 328: 1295-1297
14. Christen M, Christen B, Allan MG, Folcher M, Jenö P, Grzesiek S, Jenal U (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 (Pubitemid 47181587)
15. Christen M, Christen B, Folcher M, Schauerte A, Jenal U (2005) Identification and characterization of a cyclic di-GMP-specific phosphodiesterase and its allosteric control by GTP. J Biol Chem 280: 30829-30837 (Pubitemid 41291813)
16. Commichau FM, Stülke J (2008) Trigger enzymes: Bifuntional proteins active in metabolism and controlling gene expression. Mol Microbiol 67: 692-702 (Pubitemid 351143679)
17. Datsenko KA, Wanner BL (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Nat Acad Sci USA 97: 6640-6645 (Pubitemid 30412767)
18. Dove SL, Hochschild A (2004) A bacterial two-hybrid system based on transcription activation. Methods Mol Biol 261: 231-246
19. Dubnau D, Losick R (2006) Bistability in bacteria. Mol Microbiol 61: 564-572 (Pubitemid 44324084)
20. Duerig A, Folcher M, Abel S, Nicollier M, Schwede T, Amiot N, Giese B, Jenal U (2009) Second messenger-mediated spatiotemporal control of protein degradation regulates bacterial cell cycle progression. Genes Dev 23: 93-104
21. Fang X, Gomelsky L (2010) A post-translational, c-di-GMP-dependent mechanism regulating flagellar motility. Mol Microbiol 76: 1295-1305
22. Galperin MY (2005) A census of membrane-bound and intracellular signal transduction proteins in bacteria: Bacterial IQ, extroverts and introverts. BMC Microbiol 5: 35
23. Gardner TS, Cantor CR, Collins JJ (2000) Construction of a genetic toggle switch in Escherichia coli. Nature 403: 339-342 (Pubitemid 30062394)
24. Girgis HS, Liu Y, Ryu WS, Tavazoie S (2007) A comprehensive genetic characterization of bacterial motility. PLoS Genet 3: E154
25. Grantcharova N, Peters V, Monteiro C, Zakikhany K, Römling U (2010) Bistable expression of CsgD in biofilm development of Salmonella enterica serovar typhimurium. J Bacteriol 192: 456-466
26. Güvener ZT, Harwood CS (2007) Subcellular location characteristics of the Pseudomonas aeruginosa GGDEF protein, WspR, indicate that it produces cyclic-di-GMP in response to growth on surfaces. Mol Microbiol 66: 1459-1473 (Pubitemid 350179680)
27. Hayashi K, Morooka N, Yamamoto Y, Fujita K, Isono K, Choi S, Ohtsubo E, Baba T, Wanner BL, Mori H, Horiuchi T (2006) Highly accurate genome sequences of Escherichia coli K-12 strains MG1655 and W3110. Mol Syst Biol 2: 2006.0007
28. Hengge R (2009) Principles of cyclic-di-GMP signaling. Nat Rev Microbiol 7: 263-273
29. Hengge R (2010a) Cyclic-di-GMP reaches out into the bacterial RNA world. Sci Signal 3: Pe44
30. Hengge R (2010b) Role of c-di-GMP in the regulatory networks of Escherichia coli. In The Second Messenger Cyclic-di-GMP, Wolfe AJ, Visick KL (eds), pp 230-252. Washington, DC: ASM Press
31. Hickman JW, Harwood CS (2008) Identification of FleQ from Pseudomonas aeruginosa as a c-di-GMP-responsive transcription factor. Mol Microbiol 69: 376-389 (Pubitemid 351988011)
32. Jenal U, Malone J (2006) Mechanisms of cyclic-di-GMP signaling in bacteria. Annu Rev Genet 40: 385-407 (Pubitemid 44956791)
33. Joly N, Danot O, Schlegel A, Boos W, Richet E (2002) The Aes protein directly controls the activity of MalT, the central transcriptional activator of the Escherichia coli maltose regulon. J Biol Chem 277: 16606-16613 (Pubitemid 34967678)
34. Kader A, Simm R, Gerstel U, Morr M, Römling U (2006) Hierarchical involvement of various GGDEF domain proteins in rdar morphotype development of Salmonella enterica serovar typhimurium. Mol Microbiol 60: 602-616
35. Kulasakara H, Lee E, Brencic A, Liberati N, Urbach J, Miyata S, Lee DG, Neely AN, Hyodo M, Hayakawa Y, Ausubel FM, Lory S (2006) Analysis of Pseudomonas aeruginosa diguanylate cyclases and phosphodiesterase reveals a role for bis-(30-50)-cyclic-GMP in virulence. Proc Natl Acad Sci USA 103: 2839-2844
36. Leduc JL, Roberts G (2009) Cyclic di-GMP allosterically inhibits the CRP-like protein (Clp) of Xanthomonas axonopodis pv. citri. J Bacteriol 191: 7121-7122
37. Lee ER, Baker JL, Weinberg Z, Sudarsan N, Breaker RR (2010) An allosteric self-splicing ribozyme triggered by a bacterial second messenger. Science 329: 845-848
38. Lee VT, Matewish JM, Kessler JL, Hyodo M, Hayakawa Y, Lory S (2007) A cyclic-di-GMP receptor required for bacterial exopolysaccharide production. Mol Microbiol 65: 1474-1484 (Pubitemid 47347829)
39. Mika F, Busse S, Possling A, Berkholz J, Tschowri N, Sommerfeldt N, Pruteanu M, Hengge R (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
40. Miller JH (1972) Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory
41. Newell PD, Monds RD, Ó Toole GA (2009) LapD is a bis-(30,50)-cyclic dimeric GMP-binding protein that regulates surface attachment by Pseudomonas fluorescens Pf0-1. Proc Natl Acad Sci USA 106: 3461-3466
42. Ogasawara H, Yamada K, Kori A, Yamamoto K, Ishihama A (2010a) Regulation of the Escherichia coli csgD promoter: Interplay between five transcription factors. Microbiology 156: 2470-2483
43. Ogasawara H, Yamamoto K, Ishihama A (2010b) Regulatory role of MlrA in transcription activation of csgD, the master regulator of biofilm formation in Escherichia coli. FEMS Microbiol Lett 312: 160-168
44. Ostrovsky de Spicer P, Maloy S (1993) PutA protein, a membrane-associated flavin dehydrogenase, acts as a redoxdependent transcriptional regulator. Proc Natl Acad Sci USA 90: 4295-4298 (Pubitemid 23134213)
45. Paul K, Nieto V, Carlquist WC, Blair DF, Harshey RM (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
46. Pesavento C, Becker G, Sommerfeldt N, Possling A, Tschowri N, Mehlis A, Hengge R (2008) Inverse regulatory coordination of motility and curli-mediated adhesion in Escherichia coli. Genes Dev 22: 2434-2446
47. Römling U, Rohde M, Olsén A, Normark S, Reinköster J (2000) AgfD, the checkpoint of multicellular and aggregative behaviour in Salmonella typhimurium regulates at least two independent pathways. Mol Microbiol 36: 10-23 (Pubitemid 30195384)
48. Ryan RP, Fouhy Y, Lucey F, Dow JM (2006) Cyclic di-GMP signaling in bacteria: Recent advances and new puzzles. J Bacteriol 188: 8327-8334 (Pubitemid 44894031)
49. Ryan RP, McCarthy Y, Andrade M, Farah CS, Armitage JP, Dow JM (2010) Cell-cell signal-dependent dynamic interactions between HD-GYP and GGDEF domain proteins mediate virulence in Xanthomonas campestris. Proc Natl Acad Sci USA 107: 5989-5994
50. Schirmer T, Jenal U (2009) Structural and mechanistic determinants of c-di-GMP signalling. Nat Rev Microbiol 7: 724-735
51. Schreiber V, Steegborn C, Clausen T, Boos W, Richet E (2000) A new mechanism for the control of a prokaryotic transcriptional regulator: Antagonistic binding of positive and negative effectors. Mol Microbiol 35: 765-776 (Pubitemid 30107528)
52. Serra DO, Richter AM, Klauck G, Mika F, Hengge R (2013) Microanatomy at cellular resolution and spatial order of physiological differentiation in a bacterial biofilm. mBio 4: E00103-e00113
53. Smith KD, Lipchock SV, Ames TD, Wang J, Breaker RR, Strobel SA (2009) Structural basis of ligand binding by a c-di-GMP riboswitch. Nat Struct Mol Biol 16: 1218-1223
54. Sudarsan N, Lee ER, Weinberg Z, Moy RH, Kim JN, Link KH, Breaker RR (2008) Riboswitches in eubacteria sense the second messenger cyclic di-GMP. Science 321: 411-413 (Pubitemid 352029978)
55. Tamayo R, Pratt JT, Camilli A (2007) Roles of cyclic diguanylate in the regulation of bacterial pathogenesis. Annu Rev Microbiol 61: 131-148 (Pubitemid 350058203)
56. Tanaka Y, Kimata K, Aiba H (2000) A novel regulatory role of glucose transporter of Escherichia coli: Membrane sequestration of a global repressor Mlc. EMBO J 19: 5344-5352
57. Tuckerman JR, Gonzalez G, Gilles-Gonzalez M-A (2011) Cyclic di-GMP activation of polynucleotide phosphorylase signaldependent RNA processing. J Mol Biol 407: 633-639
58. Weber H, Pesavento C, Possling A, Tischendorf G, Hengge R (2006) Cyclic-di-GMP-mediated signaling within the sS network of Escherichia coli. Mol Microbiol 62: 1014-1034 (Pubitemid 44655315)
59. Wolfe AJ, Visick KL (eds.) (2010) The Second Messenger Cyclicdi- GMP. Washington, DC: ASM Press
60. Zdych E, Peist R, Reidl J, Boos W (1995) MalY of Escherichia coli is an enzyme with the activity of a beta C-S lyase (cystathionase). J Bacteriol 177: 5035-5039 Programme (ERC-AdG 249780)