RNA-seq analysis reveals that an ECF σ factor, AcsS, regulates achromobactin biosynthesis in pseudomonas syringae pv. syringae B728a

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Greenwald, Jessica W ^a   Greenwald, Charles J ^a   Philmus, Benjamin J ^a   Begley, Tadhg P ^a   Gross, Dennis C ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACHROMOBACTIN; EXTRACYTOPLASMIC FUNCTION SIGMA FACTOR; IRON; POLYSACCHARIDE; PYOVERDINE; SIDEROPHORE; SIGMA FACTOR; TRACE ELEMENT; TRANSCRIPTOME; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; CELL MOTILITY; DELETION MUTANT; GENE CLUSTER; GENE CONTROL; GENE EXPRESSION; NONHUMAN; PSEUDOMONAS SYRINGAE; RNA SEQUENCE;

BACTERIAL TOXINS; BIOLOGICAL TRANSPORT; CITRATES; ENVIRONMENT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENE LIBRARY; GENE ORDER; GENES, BACTERIAL; GENOME, BACTERIAL; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; IRON; KETOGLUTARIC ACIDS; MULTIGENE FAMILY; PLANT DISEASES; POLYSACCHARIDES, BACTERIAL; PSEUDOMONAS SYRINGAE; SEQUENCE ANALYSIS, RNA; SIGMA FACTOR; TRANSCRIPTOME;

EID: 84859997465     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0034804     Document Type: Article

References (59)

1. Weber KA, Achenbach LA, Coates JD, (2006) Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction. Nat Rev Microbiol 4: 752-764.
2. Koorts AM, Viljoen M, (2007) Ferritin and ferritin isoforms I: structure-function relationships, synthesis, degradation and secretion. Arch Physiol Biochem 113: 30-54.
3. Miethke M, Marahiel MA, (2007) Siderophore-based iron acquisition and pathogen control. Microbiol Mol Biol Rev 71: 413-451.
4. Joyner DC, Lindow SE, (2000) Heterogeneity of iron bioavailability on plants assessed with a whole-cell GFP-based bacterial biosensor. Microbiology 146: 2435-2445.
5. Gross DC, (1985) Regulation of syringomycin synthesis in Pseudomonas syringae pv syringae and defined conditions for its production. J Appl Bacteriol 58: 167-174.
6. Guerinot ML, (1994) Microbial iron transport. Annu Rev Microbiol 48: 743-772.
7. Jones AM, Wildermuth MC, (2011) The phytopathogen Pseudomonas syringae pv. tomato DC3000 has three high-affinity iron-scavenging systems functional under iron limitation conditions but dispensable for pathogenesis. J Bacteriol 193: 2767-2775.
8. Wensing A, Braun SD, Buttner P, Expert D, Volksch B, et al. (2010) Impact of siderophore production by Pseudomonas syringae pv. syringae 22d/93 on epiphytic fitness and biocontrol activity against Pseudomonas syringae pv. glycinea 1a/96. Appl Environ Microbiol 76: 2704-2711.
9. Franza T, Mahe B, Expert D, (2005) Erwinia chrysanthemi requires a second iron transport route dependent of the siderophore achromobactin for extracellular growth and plant infection. Mol Microbiol 55: 261-275.
10. Yang C, Gavilanes-Ruiz M, Okinaka Y, Vedel R, Berthuy I, et al. (2002) hrp genes of Erwinia chrysanthemi 3937 are important virulence factors. Mol Plant-Microbe Interact 15: 472-480.
11. Feil H, Feil WS, Chain P, Larimer F, DiBartolo G, et al. (2005) Comparison of the complete genome sequences of Pseudomonas syringae pv. syringae B728a and pv. tomato DC3000. Proc Natl Acad Sci U S A 102: 11064-11069.
12. Visca P, Imperi F, Lamont IL, (2007) Pyoverdine siderophores: from biogenesis to biosignificance. Trends Microbiol 15: 22-30.
13. Berti AD, Thomas MG, (2009) Analysis of achromobactin biosynthesis by Pseudomonas syringae pv. syringae B728a. J Bacteriol 191: 4594-4604.
14. Mossialos D, Amoutzias GD, (2007) Siderophores in fluorescent pseudomonads: new tricks from an old dog. Future Microbiol 2: 387-395.
15. Sambrook J, Fritsch EF, Maniatis T, (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Lab. Press, Plainview, NY, 2nd Ed.
16. Sawahel W, Sastry G, Knight C, Cove D, (1993) Development of an electrotransformation system for Escherichia coli DH10B. Biotechnol Tech 7: 261-266.
17. King EO, Ward MK, Raney DE, (1954) Two simple media for the demonstration of pyocyanin and fluorescin. J Lab Clin Med 44: 301-307.
18. Huynh TV, Dahlbeck D, Staskawicz BJ, (1989) Bacterial blight of soybean: regulation of a pathogen gene determining host cultivar specificity. Science 245: 1374-1377.
19. Kadurugamuwa JL, Anwar H, Brown MR, Shand GH, Ward KH, (1987) Media for study of growth kinetics and envelope properties of iron-deprived bacteria. J Clin Microbiol 25: 849-855.
20. Datsenko KA, Wanner BL, (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97: 6640-6645.
21. Records AR, Gross DC, (2010) Sensor kinases RetS and LadS regulate Pseudomonas syringae Type VI secretion and virulence factors. J Bacteriol 192: 3584-3596.
22. Landy A, (1989) Dynamic, structural, and regulatory aspects of λ site-specific recombination. Annu Rev Biochem 58: 913-949.
23. Leong SA, Ditta GS, Helinski DR, (1982) Heme biosynthesis in Rhizobium: identification of a cloned gene coding for δ-aminolevulinic acid synthetase from Rhizobium meliloti. J Biol Chem 257: 8724-8730.
24. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, et al. (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55: 611-622.
25. Jahn CE, Charkowski AO, Willis DK, (2008) Evaluation of isolation methods and RNA integrity for bacterial RNA quantitation. J Microbiol Methods 75: 318-324.
26. Lu SE, Wang N, Wang JL, Chen ZJ, Gross DC, (2005) Oligonucleotide microarray analysis of the salA regulon controlling phytotoxin production by Pseudomonas syringae pv. syringae. Mol Plant-Microbe Interact 18: 324-333.
27. Croucher NJ, Fookes MC, Perkins TT, Turner DJ, Marguerat SB, et al. (2009) A simple method for directional transcriptome sequencing using Illumina technology. Nucleic Acids Res 22: e148-e157.
28. Perkins TT, Kingsley RA, Fookes MC, Gardner PP, K.D. James KD, et al. (2009) A strand-specific RNA-seq analysis of the transcriptome of the typhoid bacillus Salmonella typhi. PLoS Genetics 5: e1000569-e1000581.
29. Kendziorski C, Irizarry RA, Chen KS, Haag JD, Gould MN, (2005) On the utility of pooling biological samples in microarray experiments. Proc Natl Acad Aci U S A 102: 4252-4257.
30. Peng X, Wood CL, Blalock EM, Chen KC, Landfield PW, et al. (2003) Statistical implications of pooling RNA samples for microarray experiments. BMC Bioinformatics 4: 26-34.
31. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B, (2008) Mapping and quantifying mammalian transcriptomes by RNA-seq. Nat Methods 5: 621-628.
32. Wang L, Feng Z, Wang X, Wang X, Zhang X, (2009) DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26: 136-138.
33. Berti AD, Greve NJ, Christensen QH, Thomas MG, (2007) Identification of a biosynthetic gene cluster and the six associated lipopeptides involved in swarming motility of Pseudomonas syringae pv. tomato DC3000. J Bacteriol 189: 6312-6323.
34. Owen JG, Ackerley DF, (2011) Characterization of pyoverdine and achromobactin in Pseudomonas syringae pv. phaseolicola 1448a. BMC Microbiol 11: 218.
35. Wang Z, Gerstein M, Snyder M, (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10: 57-63.
36. Filiatrault MJ, Stodghill PV, Bronstein PA, Moll S, Lindeberg M, et al. (2010) Transcriptome analysis of Pseudomonas syringae identifies new genes, noncoding RNAs, and antisense activity. J Bacteriol 192: 2359-2372.
37. Marioni JC, Mason CE, Mane SM, Stephens M, Gilad Y, (2008) RNA-seq: An assessment of technical reproducibility and comparison with gene expression arrays. Genome Res 18: 1509-1517.
38. Liu F, Jenssen T, Trimarchi J, Punzo C, Cepko CL, et al. (2007) Comparison of hybridization-based and sequencing-based gene expression technologies on biological replicates. BMC Genomics 8: 153-166.
39. Sorek R, Cossart P, (2010) Prokaryotic transcriptomics: a new view on regulation, physiology, and pathogenicity. Nat Rev Genet 11: 9-16.
40. Cornelis P, Bodelis J, (2009) A survey of TonB-dependent receptors in fluorescent pseudomonads. Environ Microbiol Reports 1: 256-262.
41. Anderson C, (2003) Channel-tunnels: outer membrane components of type I secretion systems and multidrug efflux pumps of gram-negative bacteria. Rev Physiol Biochem Pharmacol 147: 122-165.
42. Piddock LJV, (2006) Multidrug-resistance efflux pumps- not just for resistance. Nature Rev 4: 629-636.
43. Blair JMA, Piddock LJV, (2009) Structure, function and inhibition of RND efflux pumps in gram-negative bacteria: an update. Curr Opin Microbiol 12: 512-519.
44. Kang H, Gross DC, (2005) Characterization of a resistance-nodulation-cell division transporter system associated with the syr/syp genomic island of Pseudomonas syringae pv. syringae. Appl Environ Microbiol 71: 5056-5065.
45. Goel AK, Rajagopal L, Nagesh N, Sonti RV, (2002) Genetic locus encoding functions involved in biosynthesis and outer membrane localization of xanthomonadin in Xanthomonas oryzae pv. oryzae. J Bacteriol 184: 3539-3548.
46. Bleuel C, Grobe C, Taudte N, Scherer J, Wesenberg D, et al. (2005) TolC is involved in enterobactin efflux across the outer membrane of Escherichia coli. J Bacteriol 187: 6701-6707.
47. Arrebola E, Cazorla FM, Romero D, Peréz-Garcia A, deVicente A, (2007) A nonribosomal peptide synthetase gene (mgoA) of Pseudomonas syringae pv. syringae is involved in mangotoxin biosynthesis and is required for full virulence. Mol Plant-Microbe Interact 20: 500-509.
48. Arrebola E, Cazorla FM, Codina JC, Gutiérrez-Barranquero JA, Pérez-García A, et al. (2009) Contribution of mangotoxin to the virulence and epiphytic fitness of Pseudomonas syringae pv. syringae. Int Microbiol 12: 87-95.
49. Friedman L, Kolter R, (2004) Two genetic loci produce distinct carbohydrate-rich structural components of the Pseudomonas aeruginosa biofilm matrix. J Bacteriol 186: 4457-4465.
50. Jackson KD, Starkey M, Kremer S, Parsek MR, Wozniak DJ, (2004) Identification of psl,a locus encoding a potential exopolysaccharide that is essential for Pseudomonas aeruginosa PAO1 biofilm formation. J Bacteriol 186: 4466-4475.
51. Ma L, Lu H, Sprinkle A, Parsek MR, Wozniak DJ, (2007) Pseudomonas aeruginosa Psl is a galactose- and mannose-rich exopolysaccharide. J Bacteriol 189: 8353-8356.
52. Banin E, Vasil ML, Greenberg EP, (2005) Iron and Pseudomonas aeruginosa biofilm formation. Proc Natl Acad Sci U S A 102: 11076-11081.
53. O'Toole GA, Kolter R, (1998) Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Molecular Microbio 30: 295-304.
54. Liu R, Ochman H, (2007) Stepwise formation of the bacterial flagellar system. Proc. Natl Acad Sci U S A 104: 7116-7121.
55. 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.
56. Bernard P, Couturier M, (1992) Cell killing by the F plasmid CcdB protein involves poisoning of DNA-topoisomerase II complexes. J Mol Biol 226: 735-745.
57. Grant SGN, Jessee J, Bloom FR, Hanahan D, (1990) Differential plasmid rescue from transgenic mouse DNAs into Escherichia coli methylation restriction mutants. Proc Natl Acad Sci U S A 87: 4645-4649.
58. Loper JE, Lindow SE, (1987) Lack of evidence for in situ fluorescent pigment production by Pseudomonas syringae pv. syringae on bean leaf surfaces. Phytopathology 77: 1449-1454.
59. Hirano SS, Upper CD, (1990) Population biology and epidemiology of Pseudomonas syringae. Annu Rev Phytopathol 28: 155-177.