Identification of flgZ as a flagellar gene encoding a PilZ domain protein that regulates swimming motility and biofilm formation in Pseudomonas

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Martínez Granero, Francisco ^a   Navazo, Ana ^a   Barahona, Emma ^a   Redondo Nieto, Miguel ^a   De Heredia, Elena González ^a,b   Baena, Irene ^a   Martín Martín, Irene ^a   Rivilla, Rafael ^a   Martín, Marta ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b UNIVERSIDAD POLITÉCNICA DE MADRID   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC GMP; PHOSPHODIESTERASE; BACTERIAL PROTEIN; BIS(3',5')-CYCLIC DIGUANYLIC ACID;

ARTICLE; BIOFILM; ENZYME ACTIVITY; FLGZ GENE; GENE; GENETIC CODE; GENETIC IDENTIFICATION; NONHUMAN; OPERON; PILZ GENE; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PSEUDOMONAS; PSEUDOMONAS FLUORESCENS; SENSOR; SWIMMING; ANALOGS AND DERIVATIVES; BACTERIAL GENE; CELL FRACTIONATION; CHEMISTRY; FLAGELLUM; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOVEMENT (PHYSIOLOGY); NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE;

BACTERIAL PROTEINS; BIOFILMS; CONSERVED SEQUENCE; CYCLIC GMP; FLAGELLA; GENES, BACTERIAL; MOVEMENT; PROTEIN STRUCTURE, TERTIARY; PSEUDOMONAS; SUBCELLULAR FRACTIONS;

EID: 84895197830     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0087608     Document Type: Article

References (54)

1. Hengge R (2009) Principles of c-di-GMP signalling in bacteria. Nat Rev Microbiol 7: 263-273.
2. 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)
3. Jenal U, Malone J (2006) Mechanisms of cyclic-di-GMP signaling in bacteria. Annu Rev Genet 40: 385-407. (Pubitemid 44956791)
4. Amikam D, Galperin MY (2006) PilZ domain is part of the bacterial c-di-GMP binding protein. Bioinformatics 22: 3-6. (Pubitemid 43057001)
5. Kuchma SL, Brothers KM, Merritt JH, Liberati NT, Ausubel FM, et al. (2007) BifA, a cyclic-di-GMP phosphodiesterase, inversely regulates biofilm formation and swarming motility by Pseudomonas aeruginosa PA14. J Bacteriol 189: 8165-8178. (Pubitemid 350178928)
6. Merritt JH, Brothers KM, Kuchma SL, O'Toole GA (2007) SadC reciprocally influences biofilm formation and swarming motility via modulation of exopolysaccharide production and flagellar function. J Bacteriol 189: 8154-8164. (Pubitemid 350178927)
7. Gjermansen M, Ragas P, Tolker-Nielsen T (2006) Proteins with GGDEF and EAL domains regulate Pseudomonas putida biofilm formation and dispersal. FEMS Microbiol Lett 265: 215-224. (Pubitemid 44789686)
8. Matilla MA, Travieso ML, Ramos JL, Ramos-Gonzalez MI (2011) Cyclic diguanylate turnover mediated by the sole GGDEF/EAL response regulator in Pseudomonas putida : its role in the rhizosphere and an analysis of its target processes. Environ Microbiol 13: 1745-1766.
9. Navarro MV, Newell PD, Krasteva PV, Chatterjee D, Madden DR, et al. (2011) Structural basis for c-di-GMP-mediated inside-out signaling controlling periplasmic proteolysis. PLoS Biol 9: e1000588.
10. Newell PD, Boyd CD, Sondermann H, O'Toole GA (2011) A c-di-GMP effector system controls cell adhesion by inside-out signaling and surface protein cleavage. PLoS Biol 9: e1000587.
11. Barahona E, Navazo A, Martinez-Granero F, Zea-Bonilla T, Perez-Jimenez RM, et al. (2011) Pseudomonas fluorescens F113 mutant with enhanced competitive colonization ability and improved biocontrol activity against fungal root pathogens. Appl Environ Microbiol 77: 5412-5419.
12. Barahona E, Navazo A, Yousef-Coronado F, Aguirre de Carcer D, Martinez-Granero F, et al. (2010) Efficient rhizosphere colonization by Pseudomonas fluorescens F113 mutants unable to form biofilms on abiotic surfaces. Environ Microbiol 12: 3185-3195.
13. Capdevila S, Martinez-Granero FM, Sanchez-Contreras M, Rivilla R, Martin M (2004) Analysis of Pseudomonas fluorescens F113 genes implicated in flagellar filament synthesis and their role in competitive root colonization. Microbiology 150: 3889-3897. (Pubitemid 39545333)
14. Martinez-Granero F, Rivilla R, Martin M (2006) Rhizosphere selection of highly motile phenotypic variants of Pseudomonas fluorescens with enhanced competitive colonization ability. Appl Environ Microbiol 72: 3429-3434. (Pubitemid 43727995)
15. Sanchez-Contreras M, Martin M, Villacieros M, O'Gara F, Bonilla I, et al. (2002) Phenotypic selection and phase variation occur during alfalfa root colonization by Pseudomonas fluorescens F113. J Bacteriol 184: 1587-1596. (Pubitemid 34188211)
16. Navazo A, Barahona E, Redondo-Nieto M, Martinez-Granero F, Rivilla R, et al. (2009) Three independent signalling pathways repress motility in Pseudomonas fluorescens F113. Microb Biotechnol 2: 489-498.
17. Hickman JW, Tifrea DF, Harwood CS (2005) A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels. Proc Natl Acad Sci U S A 102: 14422-14427. (Pubitemid 41429713)
18. Ude S, Arnold DL, Moon CD, Timms-Wilson T, Spiers AJ (2006) Biofilm formation and cellulose expression among diverse environmental Pseudomonas isolates. Environ Microbiol 8: 1997-2011. (Pubitemid 44506895)
19. Spiers AJ, Bohannon J, Gehrig SM, Rainey PB (2003) Biofilm formation at the air-liquid interface by the Pseudomonas fluorescens SBW25 wrinkly spreader requires an acetylated form of cellulose. Mol Microbiol 50: 15-27. (Pubitemid 37222783)
20. Redondo-Nieto M, Barret M, Morrisey JP, Germaine K, Martinez-Granero F, et al. (2012) Genome sequence of the biocontrol strain Pseudomonas fluorescens F113. J Bacteriol 194: 1273-1274.
21. Redondo-Nieto M, Barret M, Morrissey J, Germaine K, Martinez-Granero F, et al. (2013) Genome sequence reveals that Pseudomonas fluorescens F113 possesses a large and diverse array of systems for rhizosphere function and host interaction. BMC Genomics 14: 54.
22. Boehm A, Kaiser M, Li H, Spangler C, Kasper CA, et al. (2010) Second messenger-mediated adjustment of bacterial swimming velocity. Cell 141: 107-116.
23. 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.
24. 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: 30310-30314. (Pubitemid 44582083)
25. Christen M, Christen B, Allan MG, Folcher M, Jeno P, et al. (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 U S A 104: 4112-4117. (Pubitemid 47181587)
26. Dasgupta N, Wolfgang MC, Goodman AL, Arora SK, Jyot J, et al. (2003) A four-tiered transcriptional regulatory circuit controls flagellar biogenesis in Pseudomonas aeruginosa. Mol Microbiol 50: 809-824. (Pubitemid 37372245)
27. D'Argenio DA, Calfee MW, Rainey PB, Pesci EC (2002) Autolysis and autoaggregation in Pseudomonas aeruginosa colony morphology mutants. J Bacteriol 184: 6481-6419.
28. Simm R, Morr M, Kader A, Nimtz M, Romling U (2004) GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Mol Microbiol 53: 1123-1134. (Pubitemid 39120434)
29. Christensen LD, van Gennip M, Rybtke MT, Wu H, Chiang WC, et al. (2013) Clearance of Pseudomonas aeruginosa foreign-body biofilm infections through reduction of the cyclic di-GMP level in the bacteria. Infect Immun 81: 2705-2713.
30. Li Y, Heine S, Entian M, Sauer K, Frankenberg-Dinkel N (2013) NO-induced biofilm dispersion in Pseudomonas aeruginosa is mediated by an MHYT domain-coupled phosphodiesterase. J Bacteriol 195: 3531-3542.
31. Romling U, Galperin MY, Gomelsky M (2013) Cyclic di-GMP: the first 25 years of a universal bacterial second messenger. Microbiol Mol Biol Rev 77: 1-52.
32. Krasteva PV, Giglio KM, Sondermann H (2012) Sensing the messenger: the diverse ways that bacteria signal through c-di-GMP. Protein Sci 21: 929-948.
33. Ryan RP, Tolker-Nielsen T, Dow JM (2012) When the PilZ don't work: effectors for cyclic di-GMP action in bacteria. Trends Microbiol 20: 235-242.
34. Sudarsan N, Lee ER, Weinberg Z, Moy RH, Kim JN, et al. (2008) Riboswitches in eubacteria sense the second messenger cyclic di-GMP. Science 321: 411-413. (Pubitemid 352029978)
35. Tuckerman JR, Gonzalez G, Gilles-Gonzalez MA (2011) Cyclic di-GMP activation of polynucleotide phosphorylase signal-dependent RNA processing. J Mol Biol 407: 633-639.
36. Amikam D, Benziman M (1989) Cyclic diguanylic acid and cellulose synthesis in Agrobacterium tumefaciens. J Bacteriol 171: 6649-6655. (Pubitemid 20006947)
37. Weinhouse H, Sapir S, Amikam D, Shilo Y, Volman G, et al. (1997) c-di-GMP-binding protein, a new factor regulating cellulose synthesis in Acetobacter xylinum. FEBS Lett 416: 207-211. (Pubitemid 27462790)
38. Ko J, Ryu KS, Kim H, Shin JS, Lee JO, et al. (2010) Structure of PP4397 reveals the molecular basis for different c-di-GMP binding modes by PilZ domain proteins. J Mol Biol 398: 97-110.
39. 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: 371-382.
40. Zorraquino V, Garcia B, Latasa C, Echeverz M, Toledo-Arana A, et al. (2013) Coordinated cyclic-di-GMP repression of Salmonella motility through YcgR and cellulose. J Bacteriol 195: 417-428.
41. Caiazza NC, Merritt JH, Brothers KM, O'Toole GA (2007) Inverse regulation of biofilm formation and swarming motility by Pseudomonas aeruginosa PA14. J Bacteriol 189: 3603-3612. (Pubitemid 46668825)
42. Huangyutitham V, Guvener ZT, Harwood CS (2013) Subcellular clustering of the phosphorylated WspR response regulator protein stimulates its diguanylate cyclase activity. MBio 4: e00242-00213.
43. Scher FM, Baker R (1982) Effects of Pseudomonas putida and a synthetic iron chelator on induction of soil suppressiveness to Fusarium wilt pathogens. Phytopathology 72: 1567-1573.
44. Bertani G (1951) Studies on Lysogenesis. 1. The Mode of Phage Liberation by Lysogenic Escherichia coli. J Bacteriol 62: 293-300.
45. Wilson KJ, Sessitsch A, Corbo JC, Giller KE, Akkermans AD, et al. (1995) beta-Glucuronidase (GUS) transposons for ecological and genetic studies of rhizobia and other gram-negative bacteria. Microbiology 141: 1691-1705.
46. Schäfer A, Tauch A, Jager W, Kalinowski J, Thierbach G, et al. (1994) Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene 145: 69-73. (Pubitemid 24224965)
47. Kirchner O, Tauch A (2003) Tools for genetic engineering in the amino acid-producing bacterium Corynebacterium glutamicum. J Biotechnol 104: 287-299. (Pubitemid 37011364)
48. de Lorenzo V, Eltis L, Kessler B, Timmis KN (1993) Analysis of Pseudomonas gene products using lacIq/Ptrp-lac plasmids and transposons that confer conditional phenotypes. Gene 123: 17-24. (Pubitemid 23035786)
49. Shanahan P, OSullivan DJ, Simpson P, Glennon JD, OGara F (1992) Isolation of 2,4-diacetylphloroglucinol from a fluorescent pseudomonad and investigation of physiological parameters influencing its production. Appl Environ Microbiol 58: 353-358.
50. Nakazawa T (2002) Travels of a Pseudomonas, from Japan around the world. Environ Microbiol 4: 782-786.
51. Figurski DH, Helinski DR (1979) Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc Natl Acad Sci U S A 76: 1648-1652. (Pubitemid 9175374)
52. Fletcher M (1977) The effects of culture concentration and age, time, and temperature on bacterial attachment to polystyrene. Canadian Journal of Microbiology 23: 1-6.
53. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, et al. (2009) BLAST+: architecture and applications. BMC Bioinformatics 10: 421.
54. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, et al. (2008) The RAST Server: rapid annotations using subsystems technology. BMC Genomics 9: 75.