The Single-Nucleotide Resolution Transcriptome of Pseudomonas aeruginosa Grown in Body Temperature

PLoS Pathogens

Volumn 8, Issue 9, 2012, Pages

  Wurtzel, Omri ^a   Yoder Himes, Deborah R ^b,c   Han, Kook ^b   Dandekar, Ajai A ^d   Edelheit, Sarit ^a   Greenberg, E Peter ^d   Sorek, Rotem ^a   Lory, Stephen ^b  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b HARVARD MEDICAL SCHOOL   (United States)

^c BOSTON CHILDREN S HOSPITAL   (United States)

^d UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHENAZINE; TRANSCRIPTOME;

ARTICLE; BACTERIAL GROWTH; BIOSYNTHESIS; BODY TEMPERATURE; GENE MAPPING; NONHUMAN; PATHOGENESIS; PSEUDOMONAS AERUGINOSA; RNA SEQUENCE; SINGLE NUCLEOTIDE POLYMORPHISM;

BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; BASE SEQUENCE; CHROMOSOME MAPPING; GENE EXPRESSION PROFILING; HUMANS; PHENAZINES; PROMOTER REGIONS, GENETIC; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; RNA, UNTRANSLATED; SEQUENCE ANALYSIS, DNA; TEMPERATURE; TRANS-ACTIVATORS; TRANSCRIPTOME;

MAMMALIA; PSEUDOMONAS AERUGINOSA;

EID: 84866924923     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002945     Document Type: Article

References (90)

1. Kang CI, Kim SH, Kim HB, Park SW, Choe YJ, et al. (2003) Pseudomonas aeruginosa bacteremia: risk factors for mortality and influence of delayed receipt of effective antimicrobial therapy on clinical outcome. Clin Infect Dis 37: 745-751.
2. Aaron SD, Vandemheen KL, Ramotar K, Giesbrecht-Lewis T, Tullis E, et al. (2010) Infection with transmissible strains of Pseudomonas aeruginosa and clinical outcomes in adults with cystic fibrosis. JAMA 304: 2145-2153.
3. Koh AY, Priebe GP, Ray C, Van Rooijen N, Pier GB, (2009) Inescapable need for neutrophils as mediators of cellular innate immunity to acute Pseudomonas aeruginosa pneumonia. Infect Immun 77: 5300-5310.
4. Alonso A, Rojo F, Martinez JL, (1999) Environmental and clinical isolates of Pseudomonas aeruginosa show pathogenic and biodegradative properties irrespective of their origin. Environ Microbiol 1: 421-430.
5. Oliver A, Canton R, Campo P, Baquero F, Blazquez J, (2000) High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. Science 288: 1251-1254.
6. Stover CK, Pham XQ, Erwin AL, Mizoguchi SD, Warrener P, et al. (2000) Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406: 959-964.
7. Li LL, Malone JE, Iglewski BH, (2007) Regulation of the Pseudomonas aeruginosa quorum-sensing regulator VqsR. J Bacteriol 189: 4367-4374.
8. Tan MW, Rahme LG, Sternberg JA, Tompkins RG, Ausubel FM, (1999) Pseudomonas aeruginosa killing of Caenorhabditis elegans used to identify P. aeruginosa virulence factors. Proc Natl Acad Sci U S A 96: 2408-2413.
9. Mathee K, Narasimhan G, Valdes C, Qiu X, Matewish JM, et al. (2008) Dynamics of Pseudomonas aeruginosa genome evolution. Proc Natl Acad Sci U S A 105: 3100-3105.
10. Wolfgang MC, Kulasekara BR, Liang X, Boyd D, Wu K, et al. (2003) Conservation of genome content and virulence determinants among clinical and environmental isolates of Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 100: 8484-8489.
11. Pal C, Papp B, Lercher MJ, (2005) Adaptive evolution of bacterial metabolic networks by horizontal gene transfer. Nat Genet 37: 1372-1375.
12. Cases I, de Lorenzo V, Ouzounis CA, (2003) Transcription regulation and environmental adaptation in bacteria. Trends Microbiol 11: 248-253.
13. Pallen MJ, Loman NJ, Penn CW, (2010) High-throughput sequencing and clinical microbiology: progress, opportunities and challenges. Curr Opin Microbiol 13: 625-631.
14. van Vliet AH, (2010) Next generation sequencing of microbial transcriptomes: challenges and opportunities. FEMS Microbiol Lett 302: 1-7.
15. Wurtzel O, Sapra R, Chen F, Zhu Y, Simmons BA, et al. (2010) A single-base resolution map of an archaeal transcriptome. Genome Res 20: 133-141.
16. Sharma CM, Hoffmann S, Darfeuille F, Reignier J, Findeiss S, et al. (2010) The primary transcriptome of the major human pathogen Helicobacter pylori. Nature 464: 250-255.
17. Wurtzel O, Sesto N, Mellin JR, Karunker I, Edelheit S, et al. (2012) Comparative transcriptomics of pathogenic and non-pathogenic Listeria species. Mol Syst Biol 8: 583.
18. Vijayan V, Jain IH, O'Shea EK, (2011) A high resolution map of a cyanobacterial transcriptome. Genome Biol 12: R47.
19. Sorek R, Cossart P, (2010) Prokaryotic transcriptomics: a new view on regulation, physiology and pathogenicity. Nat Rev Genet 11: 9-16.
20. Waters LS, Storz G, (2009) Regulatory RNAs in bacteria. Cell 136: 615-628.
21. Gripenland J, Netterling S, Loh E, Tiensuu T, Toledo-Arana A, et al. (2010) RNAs: regulators of bacterial virulence. Nat Rev Microbiol 8: 857-866.
22. Papenfort K, Vogel J, (2010) Regulatory RNA in bacterial pathogens. Cell Host Microbe 8: 116-127.
23. Romby P, Vandenesch F, Wagner EG, (2006) The role of RNAs in the regulation of virulence-gene expression. Curr Opin Microbiol 9: 229-236.
24. Nechooshtan G, Elgrably-Weiss M, Sheaffer A, Westhof E, Altuvia S, (2009) A pH-responsive riboregulator. Genes Dev 23: 2650-2662.
25. Wassarman KM, (2002) Small RNAs in bacteria: diverse regulators of gene expression in response to environmental changes. Cell 109: 141-144.
26. Mahenthiralingam E, Baldwin A, Dowson CG, (2008) Burkholderia cepacia complex bacteria: opportunistic pathogens with important natural biology. J Appl Microbiol 104: 1539-1551.
27. Johansson J, Mandin P, Renzoni A, Chiaruttini C, Springer M, et al. (2002) An RNA thermosensor controls expression of virulence genes in Listeria monocytogenes. Cell 110: 551-561.
28. Konkel ME, Tilly K, (2000) Temperature-regulated expression of bacterial virulence genes. Microbes Infect 2: 157-166.
29. Marceau M, (2005) Transcriptional regulation in Yersinia: an update. Curr Issues Mol Biol 7: 151-177.
30. Mereghetti L, Sitkiewicz I, Green NM, Musser JM, (2008) Remodeling of the Streptococcus agalactiae transcriptome in response to growth temperature. PLoS One 3: e2785.
31. Hauser AR, (2009) The type III secretion system of Pseudomonas aeruginosa: infection by injection. Nat Rev Microbiol 7: 654-665.
32. Fauvarque MO, Bergeret E, Chabert J, Dacheux D, Satre M, et al. (2002) Role and activation of type III secretion system genes in Pseudomonas aeruginosa-induced Drosophila killing. Microb Pathog 32: 287-295.
33. Matz C, Moreno AM, Alhede M, Manefield M, Hauser AR, et al. (2008) Pseudomonas aeruginosa uses type III secretion system to kill biofilm-associated amoebae. ISME J 2: 843-852.
34. Miyata S, Casey M, Frank DW, Ausubel FM, Drenkard E, (2003) Use of the Galleria mellonella caterpillar as a model host to study the role of the type III secretion system in Pseudomonas aeruginosa pathogenesis. Infect Immun 71: 2404-2413.
35. Brannon MK, Davis JM, Mathias JR, Hall CJ, Emerson JC, et al. (2009) Pseudomonas aeruginosa Type III secretion system interacts with phagocytes to modulate systemic infection of zebrafish embryos. Cell Microbiol 11: 755-768.
36. Clatworthy AE, Lee JS, Leibman M, Kostun Z, Davidson AJ, et al. (2009) Pseudomonas aeruginosa infection of zebrafish involves both host and pathogen determinants. Infect Immun 77: 1293-1303.
37. Rawls JF, Mahowald MA, Goodman AL, Trent CM, Gordon JI, (2007) In vivo imaging and genetic analysis link bacterial motility and symbiosis in the zebrafish gut. Proc Natl Acad Sci U S A 104: 7622-7627.
38. Wareham DW, Papakonstantinopoulou A, Curtis MA, (2005) The Pseudomonas aeruginosa PA14 type III secretion system is expressed but not essential to virulence in the Caenorhabditis elegans-P. aeruginosa pathogenicity model. FEMS Microbiol Lett 242: 209-216.
39. Cisz M, Lee PC, Rietsch A, (2008) ExoS controls the cell contact-mediated switch to effector secretion in Pseudomonas aeruginosa. J Bacteriol 190: 2726-2738.
40. Lau GW, Hassett DJ, Ran H, Kong F, (2004) The role of pyocyanin in Pseudomonas aeruginosa infection. Trends Mol Med 10: 599-606.
41. Dietrich LE, Price-Whelan A, Petersen A, Whiteley M, Newman DK, (2006) The phenazine pyocyanin is a terminal signalling factor in the quorum sensing network of Pseudomonas aeruginosa. Mol Microbiol 61: 1308-1321.
42. Wang Y, Wilks JC, Danhorn T, Ramos I, Croal L, et al. (2011) Phenazine-1-carboxylic acid promotes bacterial biofilm development via ferrous iron acquisition. J Bacteriol 193: 3606-3617.
43. Caldwell CC, Chen Y, Goetzmann HS, Hao Y, Borchers MT, et al. (2009) Pseudomonas aeruginosa exotoxin pyocyanin causes cystic fibrosis airway pathogenesis. Am J Pathol 175: 2473-2488.
44. Lau GW, Ran H, Kong F, Hassett DJ, Mavrodi D, (2004) Pseudomonas aeruginosa pyocyanin is critical for lung infection in mice. Infect Immun 72: 4275-4278.
45. Wang Y, Kern SE, Newman DK, (2010) Endogenous phenazine antibiotics promote anaerobic survival of Pseudomonas aeruginosa via extracellular electron transfer. J Bacteriol 192: 365-369.
46. Huang J, Xu Y, Zhang H, Li Y, Huang X, et al. (2009) Temperature-dependent expression of phzM and its regulatory genes lasI and ptsP in rhizosphere isolate Pseudomonas sp. strain M18. Appl Environ Microbiol 75: 6568-6580.
47. Mavrodi DV, Bonsall RF, Delaney SM, Soule MJ, Phillips G, et al. (2001) Functional analysis of genes for biosynthesis of pyocyanin and phenazine-1-carboxamide from Pseudomonas aeruginosa PAO1. J Bacteriol 183: 6454-6465.
48. Mentel M, Ahuja EG, Mavrodi DV, Breinbauer R, Thomashow LS, et al. (2009) Of two make one: the biosynthesis of phenazines. Chembiochem 10: 2295-2304.
49. Gaille C, Reimmann C, Haas D, (2003) Isochorismate synthase (PchA), the first and rate-limiting enzyme in salicylate biosynthesis of Pseudomonas aeruginosa. J Biol Chem 278: 16893-16898.
50. Oglesby AG, Farrow JM 3rd, Lee JH, Tomaras AP, Greenberg EP, et al. (2008) The influence of iron on Pseudomonas aeruginosa physiology: a regulatory link between iron and quorum sensing. J Biol Chem 283: 15558-15567.
51. Heeb S, Fletcher MP, Chhabra SR, Diggle SP, Williams P, et al. (2011) Quinolones: from antibiotics to autoinducers. FEMS Microbiol Rev 35: 247-274.
52. Rumbaugh KP, Diggle SP, Watters CM, Ross-Gillespie A, Griffin AS, et al. (2009) Quorum sensing and the social evolution of bacterial virulence. Curr Biol 19: 341-345.
53. Toledo-Arana A, Dussurget O, Nikitas G, Sesto N, Guet-Revillet H, et al. (2009) The Listeria transcriptional landscape from saprophytism to virulence. Nature 459: 950-956.
54. Qiu Y, Cho BK, Park YS, Lovley D, Palsson BO, et al. (2010) Structural and operational complexity of the Geobacter sulfurreducens genome. Genome Res 20: 1304-1311.
55. Cho BK, Zengler K, Qiu Y, Park YS, Knight EM, et al. (2009) The transcription unit architecture of the Escherichia coli genome. Nat Biotechnol 27: 1043-1049.
56. Guell M, van Noort V, Yus E, Chen WH, Leigh-Bell J, et al. (2009) Transcriptome complexity in a genome-reduced bacterium. Science 326: 1268-1271.
57. Koide T, Reiss DJ, Bare JC, Pang WL, Facciotti MT, et al. (2009) Prevalence of transcription promoters within archaeal operons and coding sequences. Mol Syst Biol 5: 285.
58. Winkler WC, Breaker RR, (2005) Regulation of bacterial gene expression by riboswitches. Annu Rev Microbiol 59: 487-517.
59. Mendoza-Vargas A, Olvera L, Olvera M, Grande R, Vega-Alvarado L, et al. (2009) Genome-wide identification of transcription start sites, promoters and transcription factor binding sites in E. coli. PLoS One 4: e7526.
60. Heurlier K, Denervaud V, Haas D, (2006) Impact of quorum sensing on fitness of Pseudomonas aeruginosa. Int J Med Microbiol 296: 93-102.
61. Schuster M, Greenberg EP, (2006) A network of networks: quorum-sensing gene regulation in Pseudomonas aeruginosa. Int J Med Microbiol 296: 73-81.
62. Williams P, Camara M, (2009) Quorum sensing and environmental adaptation in Pseudomonas aeruginosa: a tale of regulatory networks and multifunctional signal molecules. Curr Opin Microbiol 12: 182-191.
63. Schuster M, Lostroh CP, Ogi T, Greenberg EP, (2003) Identification, timing, and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: a transcriptome analysis. J Bacteriol 185: 2066-2079.
64. Wagner VE, Bushnell D, Passador L, Brooks AI, Iglewski BH, (2003) Microarray analysis of Pseudomonas aeruginosa quorum-sensing regulons: effects of growth phase and environment. J Bacteriol 185: 2080-2095.
65. Gilbert KB, Kim TH, Gupta R, Greenberg EP, Schuster M, (2009) Global position analysis of the Pseudomonas aeruginosa quorum-sensing transcription factor LasR. Mol Microbiol 73: 1072-1085.
66. Sonnleitner E, Haas D, (2011) Small RNAs as regulators of primary and secondary metabolism in Pseudomonas species. Appl Microbiol Biotechnol 91: 63-79.
67. He J, Baldini RL, Deziel E, Saucier M, Zhang Q, et al. (2004) The broad host range pathogen Pseudomonas aeruginosa strain PA14 carries two pathogenicity islands harboring plant and animal virulence genes. Proc Natl Acad Sci U S A 101: 2530-2535.
68. Padalon-Brauch G, Hershberg R, Elgrably-Weiss M, Baruch K, Rosenshine I, et al. (2008) Small RNAs encoded within genetic islands of Salmonella typhimurium show host-induced expression and role in virulence. Nucleic Acids Res 36: 1913-1927.
69. Wilderman PJ, Sowa NA, FitzGerald DJ, FitzGerald PC, Gottesman S, et al. (2004) Identification of tandem duplicate regulatory small RNAs in Pseudomonas aeruginosa involved in iron homeostasis. Proc Natl Acad Sci U S A 101: 9792-9797.
70. Lee VT, Smith RS, Tummler B, Lory S, (2005) Activities of Pseudomonas aeruginosa effectors secreted by the Type III secretion system in vitro and during infection. Infect Immun 73: 1695-1705.
71. Rietsch A, Vallet-Gely I, Dove SL, Mekalanos JJ, (2005) ExsE, a secreted regulator of type III secretion genes in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 102: 8006-8011.
72. Thaden JT, Lory S, Gardner TS, (2010) Quorum-sensing regulation of a copper toxicity system in Pseudomonas aeruginosa. J Bacteriol 192: 2557-2568.
73. Furste JP, Pansegrau W, Frank R, Blocker H, Scholz P, et al. (1986) Molecular cloning of the plasmid RP4 primase region in a multi-host-range tacP expression vector. Gene 48: 119-131.
74. Hoang HH, Nickerson NN, Lee VT, Kazimirova A, Chami M, et al. (2011) Outer membrane targeting of Pseudomonas aeruginosa proteins shows variable dependence on the components of Bam and Lol machineries. MBio 2: 00246-11.
75. Nicas TI, Iglewski BH, (1985) The contribution of exoproducts to virulence of Pseudomonas aeruginosa. Can J Microbiol 31: 387-392.
76. Yoder-Himes DR, Chain PS, Zhu Y, Wurtzel O, Rubin EM, et al. (2009) Mapping the Burkholderia cenocepacia niche response via high-throughput sequencing. Proc Natl Acad Sci U S A 106: 3976-3981.
77. He S, Wurtzel O, Singh K, Froula JL, Yilmaz S, et al. (2010) Validation of two ribosomal RNA removal methods for microbial metatranscriptomics. Nat Methods 7: 807-812.
78. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B, (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5: 621-628.
79. Bauer S, Grossmann S, Vingron M, Robinson PN, (2008) Ontologizer 2.0-a multifunctional tool for GO term enrichment analysis and data exploration. Bioinformatics 24: 1650-1651.
80. Houseley J, Tollervey D, (2009) The many pathways of RNA degradation. Cell 136: 763-776.
81. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, et al. (2009) BLAST+: architecture and applications. BMC Bioinformatics 10: 421.
82. Kingsford CL, Ayanbule K, Salzberg SL, (2007) Rapid, accurate, computational discovery of Rho-independent transcription terminators illuminates their relationship to DNA uptake. Genome Biol 8: R22.
83. Munch R, Hiller K, Barg H, Heldt D, Linz S, et al. (2003) PRODORIC: prokaryotic database of gene regulation. Nucleic Acids Res 31: 266-269.
84. Turatsinze JV, Thomas-Chollier M, Defrance M, van Helden J, (2008) Using RSAT to scan genome sequences for transcription factor binding sites and cis-regulatory modules. Nat Protoc 3: 1578-1588.
85. Urban JH, Vogel J, (2008) Two seemingly homologous noncoding RNAs act hierarchically to activate glmS mRNA translation. PLoS Biol 6: e64.
86. Schuster M, Urbanowski ML, Greenberg EP, (2004) Promoter specificity in Pseudomonas aeruginosa quorum sensing revealed by DNA binding of purified LasR. Proc Natl Acad Sci U S A 101: 15833-15839.
87. Hopkins JF, Panja S, McNeil SA, Woodson SA, (2009) Effect of salt and RNA structure on annealing and strand displacement by Hfq. Nucleic Acids Res 37: 6205-6213.
88. Hoang TT, Kutchma AJ, Becher A, Schweizer HP, (2000) Integration-proficient plasmids for Pseudomonas aeruginosa: site-specific integration and use for engineering of reporter and expression strains. Plasmid 43: 59-72.
89. Chen L, Xiong Z, Sun L, Yang J, Jin Q, (2012) VFDB 2012 update: toward the genetic diversity and molecular evolution of bacterial virulence factors. Nucleic Acids Res 40: D641-645.
90. Schuster M, Greenberg EP, (2007) Early activation of quorum sensing in Pseudomonas aeruginosa reveals the architecture of a complex regulon. BMC Genomics 8: 287.