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Escherichia coli K-12 substr. MG1655 Polypeptide: molecular brake that regulates flagellar motility in response to c-di-GMP



Gene: ycgR Accession Numbers: G6623 (EcoCyc), b1194, ECK1182

Regulation Summary Diagram: ?

Summary:
YcgR regulates flagellar motility in a c-di-GMP-dependent manner in vivo [Ryjenkov06]. YcgR acts as a molecular brake that interacts with the flagellar switch complex proteins FliG [Paul10, Fang10] and FliM [Paul10]. Published evidence is contradictory regarding whether binding the flagellar switch complex proteins is c-di-GMP-dependent [Paul10] or only strengthened by c-di-GMP [Fang10], and whether [Boehm10] or not [Paul10] YcgR interacts directly with the MotA flagellar motor protein. Entry into stationary phase initiates production of increased levels of c-di-GMP, which binds to YcgR and thereby leads to slower flagellar motor speeds [Boehm10, Paul10] and increased counter-clockwise flagellar rotation bias [Paul10, Fang10].

Purified YcgR specifically binds one c-di-GMP dimer per YcgR monomer with a Kd of 0.84 µM in vitro; the PilZ domain is sufficient for binding activity [Amikam06, Ryjenkov06]. An R118D mutant is unable to bind c-di-GMP [Ryjenkov06].

ycgR mutations suppress the flagellar motility defect of an hns mutant [Ko00a] and a yhjH mutant [Girgis07, Fang10] and the swarming defect of a yfiR mutant [Girgis07]. Point mutations in ycgR that weaken the interaction between YcgR and FliG allow improved motility of an hns deletion strain [Paul11]. ycgR null mutant swims faster than the wild type organism at entry into stationary phase [Boehm10].

Expression of ycgR requires FlhDC [Ko00a].

Reviews: [Wolfe08, Schirmer09, Armitage10, Guttenplan13]

Citations: [Hou13]

Locations: cell projection

Map Position: [1,243,016 <- 1,243,750] (26.79 centisomes)
Length: 735 bp / 244 aa

Molecular Weight of Polypeptide: 27.857 kD (from nucleotide sequence)

Unification Links: ASAP:ABE-0004009 , DIP:DIP-11561N , EchoBASE:EB3658 , EcoGene:EG13899 , EcoliWiki:b1194 , OU-Microarray:b1194 , PortEco:ycgR , Pride:P76010 , Protein Model Portal:P76010 , RefSeq:NP_415712 , RegulonDB:G6623 , SMR:P76010 , String:511145.b1194 , UniProt:P76010

Relationship Links: InterPro:IN-FAMILY:IPR009875 , InterPro:IN-FAMILY:IPR009926 , InterPro:IN-FAMILY:IPR012349 , InterPro:IN-FAMILY:IPR023787 , Pfam:IN-FAMILY:PF07238 , Pfam:IN-FAMILY:PF07317

Genetic Regulation Schematic: ?

GO Terms:

Biological Process: GO:0051270 - regulation of cellular component movement Inferred from experiment [Girgis07]
GO:0071945 - regulation of bacterial-type flagellum-dependent cell motility by regulation of motor speed Inferred from experiment Inferred by computational analysis [GOA06, GOA01a, Paul10]
GO:0071973 - bacterial-type flagellum-dependent cell motility Inferred from experiment Inferred by computational analysis [GOA06, Ko00a, Girgis07]
GO:0055114 - oxidation-reduction process Inferred by computational analysis [GOA01a]
Molecular Function: GO:0005515 - protein binding Inferred from experiment [Paul10]
GO:0035438 - cyclic-di-GMP binding Inferred from experiment Inferred by computational analysis [GOA06, GOA01a, Ryjenkov06]
GO:0000166 - nucleotide binding Inferred by computational analysis [UniProtGOA11a]
GO:0010181 - FMN binding Inferred by computational analysis [GOA01a]
GO:0016491 - oxidoreductase activity Inferred by computational analysis [GOA01a]
Cellular Component: GO:0009288 - bacterial-type flagellum Inferred by computational analysis [UniProtGOA11a]
GO:0009425 - bacterial-type flagellum basal body Inferred by computational analysis [UniProtGOA11]

MultiFun Terms: cell processes motility, chemotaxis, energytaxis (aerotaxis, redoxtaxis etc)
regulation

Essentiality data for ycgR knockouts: ?

Growth Medium Growth? T (°C) O2 pH Osm/L Growth Observations
LB enriched Yes 37 Aerobic 6.95   Yes [Gerdes03, Comment 1]
LB Lennox Yes 37 Aerobic 7   Yes [Baba06, Comment 2]
M9 medium with 1% glycerol Yes 37 Aerobic 7.2 0.35 Yes [Joyce06, Comment 3]
MOPS medium with 0.4% glucose Yes 37 Aerobic 7.2 0.22 Yes [Baba06, Comment 2]

Credits:
Last-Curated ? 10-Jun-2013 by Keseler I , SRI International


Sequence Features

Feature Class Location Citations Comment
Mutagenesis-Variant 42
[Paul10, UniProt11]
Alternate sequence: K → D; UniProt: Suppression of the yhjH disruption motility phenotype.
Mutagenesis-Variant 62
[Paul10, UniProt11]
Alternate sequence: N → W; UniProt: Signficant suppression of the yhjH disruption motility phenotype, less binding to FliG.
Mutagenesis-Variant 81
[Paul10, UniProt11]
Alternate sequence: K → D; UniProt: Signficant suppression of the yhjH disruption motility phenotype, less binding to FliG.
Conserved-Region 112 -> 230
[UniProt10]
UniProt: PilZ;
Mutagenesis-Variant 118
[Ryjenkov06, UniProt11]
Alternate sequence: R → D; UniProt: Complete loss of c-di-GMP binding in vitro, suppresses yhjH disruption (PubMed:16920715). Somewhat reduced binding to FliM, stimulated by c-di-GMP, greatly reduced binding to FliG (PubMed:20346719).
Mutagenesis-Variant 147
[Ryjenkov06, UniProt11]
Alternate sequence: S → A; UniProt: Slight increase in affinity for c- di-GMP.
Mutagenesis-Variant 223
[Paul10, UniProt11]
Alternate sequence: Q → W; UniProt: Signficant suppression of the yhjH disruption motility phenotype.
Alternate sequence: Q → P; UniProt: Signficant suppression of the yhjH disruption motility phenotype, no binding to FliM.
Mutagenesis-Variant 227
[Paul10, UniProt11]
Alternate sequence: I → W; UniProt: Some suppression of the yhjH disruption motility phenotype, no binding to FliM.


Gene Local Context (not to scale): ?

Transcription Unit:

Notes:

History:
Markus Krummenacker on Tue Oct 14, 1997:
Gene object created from Blattner lab Genbank (v. M52) entry.


References

Amikam06: Amikam D, Galperin MY (2006). "PilZ domain is part of the bacterial c-di-GMP binding protein." Bioinformatics 22(1);3-6. PMID: 16249258

Armitage10: Armitage JP, Berry RM (2010). "Time for bacteria to slow down." Cell 141(1);24-6. PMID: 20371342

Baba06: Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, Datsenko KA, Tomita M, Wanner BL, Mori H (2006). "Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection." Mol Syst Biol 2;2006.0008. PMID: 16738554

Boehm10: Boehm A, Kaiser M, Li H, Spangler C, Kasper CA, Ackermann M, Kaever V, Sourjik V, Roth V, Jenal U (2010). "Second messenger-mediated adjustment of bacterial swimming velocity." Cell 141(1);107-16. PMID: 20303158

Fang10: Fang X, Gomelsky M (2010). "A post-translational, c-di-GMP-dependent mechanism regulating flagellar motility." Mol Microbiol 76(5);1295-305. PMID: 20444091

Gerdes03: Gerdes SY, Scholle MD, Campbell JW, Balazsi G, Ravasz E, Daugherty MD, Somera AL, Kyrpides NC, Anderson I, Gelfand MS, Bhattacharya A, Kapatral V, D'Souza M, Baev MV, Grechkin Y, Mseeh F, Fonstein MY, Overbeek R, Barabasi AL, Oltvai ZN, Osterman AL (2003). "Experimental determination and system level analysis of essential genes in Escherichia coli MG1655." J Bacteriol 185(19);5673-84. PMID: 13129938

Girgis07: Girgis HS, Liu Y, Ryu WS, Tavazoie S (2007). "A comprehensive genetic characterization of bacterial motility." PLoS Genet 3(9);1644-60. PMID: 17941710

GOA01a: GOA, DDB, FB, MGI, ZFIN (2001). "Gene Ontology annotation through association of InterPro records with GO terms."

GOA06: GOA, SIB (2006). "Electronic Gene Ontology annotations created by transferring manual GO annotations between orthologous microbial proteins."

Guttenplan13: Guttenplan SB, Kearns DB (2013). "Regulation of flagellar motility during biofilm formation." FEMS Microbiol Rev 37(6);849-71. PMID: 23480406

Hou13: Hou Y, Li de F, Wang da C (2013). "Crystallization and preliminary X-ray analysis of the flagellar motor `brake' molecule YcgR with c-di-GMP from Escherichia coli." Acta Crystallogr Sect F Struct Biol Cryst Commun 69(Pt 6);663-5. PMID: 23722848

Joyce06: Joyce AR, Reed JL, White A, Edwards R, Osterman A, Baba T, Mori H, Lesely SA, Palsson BO, Agarwalla S (2006). "Experimental and computational assessment of conditionally essential genes in Escherichia coli." J Bacteriol 188(23);8259-71. PMID: 17012394

Ko00a: Ko M, Park C (2000). "Two novel flagellar components and H-NS are involved in the motor function of Escherichia coli." J Mol Biol 303(3);371-82. PMID: 11031114

Paul10: 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(1):128-39. PMID: 20346719

Paul11: Paul K, Carlquist WC, Blair DF (2011). "Adjusting the spokes of the flagellar motor with the DNA-binding protein H-NS." J Bacteriol 193(21);5914-22. PMID: 21890701

Ryjenkov06: Ryjenkov DA, Simm R, Romling U, Gomelsky M (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(41):30310-4. PMID: 16920715

Schirmer09: Schirmer T, Jenal U (2009). "Structural and mechanistic determinants of c-di-GMP signalling." Nat Rev Microbiol 7(10);724-35. PMID: 19756011

UniProt10: UniProt Consortium (2010). "UniProt version 2010-11 released on 2010-11-02 00:00:00." Database.

UniProt11: UniProt Consortium (2011). "UniProt version 2011-06 released on 2011-06-30 00:00:00." Database.

UniProtGOA11: UniProt-GOA (2011). "Gene Ontology annotation based on the manual assignment of UniProtKB Subcellular Location terms in UniProtKB/Swiss-Prot entries."

UniProtGOA11a: UniProt-GOA (2011). "Gene Ontology annotation based on manual assignment of UniProtKB keywords in UniProtKB/Swiss-Prot entries."

Wolfe08: Wolfe AJ, Visick KL (2008). "Get the message out: cyclic-Di-GMP regulates multiple levels of flagellum-based motility." J Bacteriol 190(2);463-75. PMID: 17993515

Other References Related to Gene Regulation

Zhao07: Zhao K, Liu M, Burgess RR (2007). "Adaptation in bacterial flagellar and motility systems: from regulon members to 'foraging'-like behavior in E. coli." Nucleic Acids Res 35(13);4441-52. PMID: 17576668


Report Errors or Provide Feedback
Please cite the following article in publications resulting from the use of EcoCyc: Nucleic Acids Research 41:D605-12 2013
Page generated by SRI International Pathway Tools version 18.5 on Sat Dec 20, 2014, biocyc14.