Novel genes involved in Pseudomonas fluorescens Pf0-1 motility and biofilm formation

Applied and Environmental Microbiology

Volumn 78, Issue 12, 2012, Pages 4318-4329

  Mastropaolo, Matthew D ^a   Silby, Mark W ^a,b   Nicoll, Julie S ^a   Levy, Stuart B ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MASSACHUSETTS DARTMOUTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOFILM FORMATION; BROTH CULTURE; DELETION MUTANTS; DIFFERENT EFFECTS; GENE EXPRESSION PATTERNS; GLYCOSYL TRANSFERASE; ORTHOLOGS; P.AERUGINOSA; PSEUDOMONAS FLUORESCENS; TRANSCRIPTOMES; WILD TYPES;

BACTERIA; BIOFILMS; CELLS;

GENE EXPRESSION;

BETA GALACTOSIDASE;

BACTERIUM; BIOFILM; COMPLEXITY; GENE EXPRESSION; MOTILITY; PERSISTENCE; PROTEIN; VIRULENCE;

ARTICLE; BACTERIAL GENE; BIOFILM; GENE DELETION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE FUSION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LOCOMOTION; MICROARRAY ANALYSIS; PHYSIOLOGY; PSEUDOMONAS FLUORESCENS; REPORTER GENE;

ARTIFICIAL GENE FUSION; BETA-GALACTOSIDASE; BIOFILMS; GENE DELETION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; GENES, REPORTER; LOCOMOTION; MICROARRAY ANALYSIS; PSEUDOMONAS FLUORESCENS;

PSEUDOMONAS; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS FLUORESCENS; PSEUDOMONAS SYRINGAE;

EID: 84864076991     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.07201-11     Document Type: Article

References (67)

1. Albert-Weissenberger C, et al. 2010. Control of flagellar gene regulation in Legionella pneumophila and its relation to growth phase. J. Bacteriol. 192:446-455.
2. Arora SK, Neely AN, Blair B, Lory S, Ramphal R. 2005. Role of motility and flagellin glycosylation in the pathogenesis of Pseudomonas aeruginosa burn wound infections. Infect. Immun. 73:4395-4398.
3. Arora SK, Ritchings BW, Almira EC, Lory S, Ramphal R. 1997. A transcriptional activator, FleQ, regulates mucin adhesion and flagellar gene expression in Pseudomonas aeruginosa in a cascade manner. J. Bacteriol. 179:5574-5581.
4. Beatson SA, Whitchurch CB, Sargent JL, Levesque RC, Mattick JS. 2002. Differential regulation of twitching motility and elastase production by Vfr in Pseudomonas aeruginosa. J. Bacteriol. 184:3605-3613.
5. Caiazza NC, O'Toole GA. 2004. SadB is required for the transition from reversible to irreversible attachment during biofilm formation by Pseudomonas aeruginosa PA14. J. Bacteriol. 186:4476-4485.
6. Caiazza NC, Shanks RM, O'Toole GA. 2005. Rhamnolipids modulate swarming motility patterns of Pseudomonas aeruginosa. J. Bacteriol. 187: 7351-7361.
7. 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.
8. Casaz P, et al. 2001. The Pseudomonas fluorescens transcription activator AdnA is required for adhesion and motility. Microbiology 147:355-361.
9. Choi KH, Kumar A, Schweizer HP. 2006. A 10-min method for preparation of highly electrocompetent Pseudomonas aeruginosa cells: application for DNA fragment transfer between chromosomes and plasmid transformation. J. Microbiol. Methods 64:391-397.
10. Compeau G, Al-Achi BJ, Platsouka E, Levy SB. 1988. Survival of rifampin-resistant mutants of Pseudomonas fluorescens and Pseudomonas putida in soil systems. Appl. Environ. Microbiol. 54:2432-2438.
11. Dasgupta N, Arora SK, Ramphal R. 2000. fleN, a gene that regulates flagellar number in Pseudomonas aeruginosa. J. Bacteriol. 182:357-364.
12. Dasgupta N, Ferrell EP, Kanack KJ, West SE, Ramphal R. 2002. fleQ, the gene encoding the major flagellar regulator of Pseudomonas aeruginosa, is _70 dependent and is downregulated by Vfr, a homolog of Escherichia coli cyclic AMP receptor protein. J. Bacteriol. 184:5240-5250.
13. Dasgupta N, et al. 2003. A four-tiered transcriptional regulatory circuit controls flagellar biogenesis in Pseudomonas aeruginosa. Mol. Microbiol. 50:809-824.
14. Deflaun MF, Marshall BM, Kulle EP, Levy SB. 1994. Tn5 insertion mutants of Pseudomonas fluorescens defective in adhesion to soil and seeds. Appl. Environ. Microbiol. 60:2637-2642.
15. Deflaun MF, Tanzer AS, McAteer AL, Marshall B, Levy SB. 1990. Development of an adhesion assay and characterization of an adhesiondeficient mutant of Pseudomonas fluorescens. Appl. Environ. Microbiol. 56:112-119.
16. de Lorenzo V, Fernandez S, Herrero M, Jakubzik U, Timmis KN. 1993. Engineering of alkyl- and haloaromatic-responsive gene expression with mini-transposons containing regulated promoters of biodegradative pathways of Pseudomonas. Gene 130:41-46.
17. Farinha MA, Ronald SL, Kropinski AM, Paranchych W. 1993. Localization of the virulence-associated genes pilA, pilR, rpoN, fliA, fliC, ent, and fbp on the physical map of Pseudomonas aeruginosa PAO1 by pulsed-field electrophoresis. Infect. Immun. 61:1571-1575.
18. Garbeva P, Silby MW, Raaijmakers JM, Levy SB, Boer WD. 2011. Transcriptional and antagonistic responses of Pseudomonas fluorescens Pf0-1 to phylogenetically different bacterial competitors. ISME J. 5:973-985.
19. Garrett ES, Perlegas D, Wozniak DJ. 1999. Negative control of flagellum synthesis in Pseudomonas aeruginosa is modulated by the alternative sigma factor AlgT (AlgU). J. Bacteriol. 181:7401-7404.
20. Gegner JA, Dahlquist FW. 1991. Signal transduction in bacteria: CheW forms a reversible complex with the protein kinase CheA. Proc. Natl. Acad. Sci. U. S. A. 88:750-754.
21. Hanahan D. 1983. Studies on transformation of Escherichia coli with plasmids. J. Mol. Biol. 166:557-580.
22. Harshey RM. 1994. Bees aren't the only ones: swarming in gram-negative bacteria. Mol. Microbiol. 13:389-394.
23. Hassan KA, et al. 2010. Inactivation of the GacA response regulator in Pseudomonas fluorescens Pf-5 has far-reaching transcriptomic consequences. Environ. Microbiol. 12:899-915.
24. Horton RM, Hunt HD, Ho SN, Pullen JK, Pease LR. 1989. Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension. Gene 77:61-68.
25. Kato J, Nakamura T, Kuroda A, Ohtake H. 1999. Cloning and characterization of chemotaxis genes in Pseudomonas aeruginosa. Biosci. Biotechnol. Biochem. 63:155-161.
26. Kim YK, McCarter LL. 2000. Analysis of the polar flagellar gene system of Vibrio parahaemolyticus. J. Bacteriol. 182:3693-3704.
27. Kirner S, et al. 1996. The non-haem chloroperoxidase from Pseudomonas fluorescens and its relationship to pyrrolnitrin biosynthesis. Microbiology 142(Pt 8):2129-2135.
28. Klose KE, Mekalanos JJ. 1998. Distinct roles of an alternative sigma factor during both free-swimming and colonizing phases of the Vibrio cholerae pathogenic cycle. Mol. Microbiol. 28:501-520.
29. Kovach ME, et al. 1995. Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166:175-176.
30. Kutsukake K. 1997. Autogenous and global control of the flagellar master operon, flhD, in Salmonella typhimurium. Mol. Gen. Genet. 254:440-448.
31. Lajoie CA, Zylstra GJ, DeFlaun MF, Strom PF. 1993. Development of field application vectors for bioremediation of soils contaminated with polychlorinated biphenyls. Appl. Environ. Microbiol. 59:1735-1741.
32. Logan SM. 2006. Flagellar glycosylation-a new component of the motility repertoire? Microbiology 152:1249-1262.
33. Marshall B, et al. 2001. The adnA transcriptional factor affects persistence and spread of Pseudomonas fluorescens under natural field conditions. Appl. Environ. Microbiol. 67:852-857.
34. Martinez RM, Jude BA, Kirn TJ, Skorupski K, Taylor RK. 2010. Role of FlgT in anchoring the flagellum of Vibrio cholerae. J. Bacteriol. 192:2085-2092.
35. Matthews M, Roy CR. 2000. Identification and subcellular localization of the Legionella pneumophila IcmX protein: a factor essential for establishment of a replicative organelle in eukaryotic host cells. Infect. Immun. 68:3971-3982.
36. 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.
37. Miller JH. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
38. Nambu T, Minamino T, Macnab RM, Kutsukake K. 1999. Peptidoglycan-hydrolyzing activity of the FlgJ protein, essential for flagellar rod formation in Salmonella typhimurium. J. Bacteriol. 181:1555-1561.
39. Navazo A, et al. 2009. Three independent signalling pathways repress motility in Pseudomonas fluorescens F113. Microb. Biotechnol. 2:489-498.
40. O'Toole GA, Kolter R. 1998. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 30:295-304.
41. O'Toole GA, Kolter R. 1998. Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol. Microbiol. 28:449-461.
42. Overhage J, Bains M, Brazas MD, Hancock RE. 2008. Swarming of Pseudomonas aeruginosa is a complex adaptation leading to increased production of virulence factors and antibiotic resistance. J. Bacteriol. 190: 2671-2679.
43. Overhage J, Lewenza S, Marr AK, Hancock RE. 2007. Identification of genes involved in swarming motility using a Pseudomonas aeruginosa PAO1 mini-Tn5-lux mutant library. J. Bacteriol. 189:2164-2169.
44. Qiu D, Damron FH, Mima T, Schweizer HP, Yu HD. 2008. PBAD-based shuttle vectors for functional analysis of toxic and highly regulated genes in Pseudomonas and Burkholderia spp. and other bacteria. Appl. Environ. Microbiol. 74:7422-7426.
45. Rainey PB. 1999. Adaptation of Pseudomonas fluorescens to the plant rhizosphere. Environ. Microbiol. 1:243-257.
46. Redondo-Nieto M, et al. 2008. Transcriptional organization of the region encoding the synthesis of the flagellar filament in Pseudomonas fluorescens. J. Bacteriol. 190:4106-4109.
47. Ritchings BW, Almira EC, Lory S, Ramphal R. 1995. Cloning and phenotypic characterization of fleS and fleR, new response regulators of Pseudomonas aeruginosa which regulate motility and adhesion to mucin. Infect. Immun. 63:4868-4876.
48. Robleto EA, Lopez-Hernandez I, Silby MW, Levy SB. 2003. Genetic analysis of the AdnA regulon in Pseudomonas fluorescens: nonessential role of flagella in adhesion to sand and biofilm formation. J. Bacteriol. 185: 453-460.
49. Sambrook J, Russell DW. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
50. Shanks RM, Caiazza NC, Hinsa SM, Toutain CM, O'Toole GA. 2006. Saccharomyces cerevisiae-based molecular tool kit for manipulation of genes from gram-negative bacteria. Appl. Environ. Microbiol. 72:5027-5036.
51. Silby MW, et al. 2009. Genomic and genetic analyses of diversity and plant interactions of Pseudomonas fluorescens. Genome Biol. 10:R51. doi: 10.1186/gb-2009-10-5-r51.
52. Silby MW, Levy SB. 2008. Overlapping protein-encoding genes in Pseudomonas fluorescens Pf0-1. PLoS Genet. 4:e1000094. doi:10.1371/ journal.pgen.1000094.
53. Silby MW, Levy SB. 2004. Use of in vivo expression technology to identify genes important in growth and survival of Pseudomonas fluorescens Pf0-1 in soil: discovery of expressed sequences with novel genetic organization. J. Bacteriol. 186:7411-7419.
54. Silby MW, Nicoll JS, Levy SB. 2009. Requirement of polyphosphate by Pseudomonas fluorescens Pf0-1 for competitive fitness and heat tolerance in laboratory media and sterile soil. Appl. Environ. Microbiol. 75:3872-3881.
55. Simon R, Priefer U, Puhler A. 1983. A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram negative bacteria. Biotechnology (NY) 1:784-791.
56. Simons M, et al. 1996. Gnotobiotic system for studying rhizosphere colonization by plant growth-promoting Pseudomonas bacteria. Mol. Plant Microbe Interact. 9:600-607.
57. Skorupski K, Taylor RK. 1997. Cyclic AMP and its receptor protein negatively regulate the coordinate expression of cholera toxin and toxincoregulated pilus in Vibrio cholerae. Proc. Natl. Acad. Sci. U. S. A. 94:265-270.
58. Spohn G, Scarlato V. 1999. Motility of Helicobacter pylori is coordinately regulated by the transcriptional activator FlgR, an NtrC homolog. J. Bacteriol. 181:593-599.
59. Starnbach MN, Lory S. 1992. The fliA (rpoF) gene of Pseudomonas aeruginosa encodes an alternative sigma factor required for flagellin synthesis. Mol. Microbiol. 6:459-469.
60. Taguchi F, et al. 2008. Effects of glycosylation on swimming ability and flagellar polymorphic transformation in Pseudomonas syringae pv. tabaci 6605. J. Bacteriol. 190:764-768.
61. Taguchi F, et al. 2006. Identification of glycosylation genes and glycosylated amino acids of flagellin in Pseudomonas syringae pv. tabaci. Cell. Microbiol. 8:923-938.
62. Takeuchi K, et al. 2003. Flagellin glycosylation island in Pseudomonas syringae pv. glycinea and its role in host specificity. J. Bacteriol. 185:6658-6665.
63. Tart AH, Blanks MJ, Wozniak DJ. 2006. The AlgT-dependent transcriptional regulator AmrZ (AlgZ) inhibits flagellum biosynthesis in mucoid, nonmotile Pseudomonas aeruginosa cystic fibrosis isolates. J. Bacteriol. 188:6483-6489.
64. Tart AH, Wolfgang MC, Wozniak DJ. 2005. The alternative sigma factor AlgT represses Pseudomonas aeruginosa flagellum biosynthesis by inhibiting expression of fleQ. J. Bacteriol. 187:7955-7962.
65. Totten PA, Lara JC, Lory S. 1990. The rpoN gene product of Pseudomonas aeruginosa is required for expression of diverse genes, including the flagellin gene. J. Bacteriol. 172:389-396.
66. Van Houdt R, Michiels CW. 2010. Biofilm formation and the food industry, a focus on the bacterial outer surface. J. Appl. Microbiol. 109: 1117-1131.
67. West SE, Sample AK, Runyen-Janecky LJ. 1994. The vfr gene product, required for Pseudomonas aeruginosa exotoxin A and protease production, belongs to the cyclic AMP receptor protein family. J. Bacteriol. 176: 7532-7542.