1887

Abstract

Bacteria contain small non-coding RNAs (ncRNAs) that are responsible for altering transcription, translation or mRNA stability. ncRNAs are important because they regulate virulence factors and susceptibility to various stresses. Here, the regulation of a recently described ncRNA of pv. DC3000, , was investigated. We determined that RpoS regulates the expression of . We found that deletion of results in increased sensitivity to hydrogen peroxide compared to the wild-type strain, suggesting that plays a role in the bacteria’s susceptibility to oxidative stress. Additionally the mutant displayed enhanced resistance to heat stress. Our findings provide new information on the regulation and role of this ncRNA in .

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2013-02-01
2020-08-14
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References

  1. Altier C., Suyemoto M., Lawhon S. D.. ( 2000;). Regulation of Salmonella enterica serovar Typhimurium invasion genes by csrA . Infect Immun68:6790–6797 [CrossRef][PubMed]
    [Google Scholar]
  2. Alvarez M. E., Pennell R. I., Meijer P. J., Ishikawa A., Dixon R. A., Lamb C.. ( 1998;). Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell92:773–784 [CrossRef][PubMed]
    [Google Scholar]
  3. Battesti A., Majdalani N., Gottesman S.. ( 2011;). The RpoS-mediated general stress response in Escherichia coli . Annu Rev Microbiol65:189–213 [CrossRef][PubMed]
    [Google Scholar]
  4. Berghoff B. A., Glaeser J., Sharma C. M., Zobawa M., Lottspeich F., Vogel J., Klug G.. ( 2011;). Contribution of Hfq to photooxidative stress resistance and global regulation in Rhodobacter sphaeroides . Mol Microbiol80:1479–1495 [CrossRef][PubMed]
    [Google Scholar]
  5. Bolwell G. P.. ( 1999;). Role of active oxygen species and NO in plant defence responses. Curr Opin Plant Biol2:287–294 [CrossRef][PubMed]
    [Google Scholar]
  6. Bronstein P. A., Filiatrault M. J., Myers C. R., Rutzke M., Schneider D. J., Cartinhour S. W.. ( 2008;). Global transcriptional responses of Pseudomonas syringae DC3000 to changes in iron bioavailability in vitro. BMC Microbiol8:209 [CrossRef][PubMed]
    [Google Scholar]
  7. Browman D. T., Hoegg M. B., Robbins S. M.. ( 2007;). The SPFH domain-containing proteins: more than lipid raft markers. Trends Cell Biol17:394–402 [CrossRef][PubMed]
    [Google Scholar]
  8. Burrowes E., Abbas A., O’Neill A., Adams C., O’Gara F.. ( 2005;). Characterisation of the regulatory RNA RsmB from Pseudomonas aeruginosa PAO1. Res Microbiol156:7–16 [CrossRef][PubMed]
    [Google Scholar]
  9. Butcher B. G., Helmann J. D.. ( 2006;). Identification of Bacillus subtilis sigma-dependent genes that provide intrinsic resistance to antimicrobial compounds produced by bacilli. Mol Microbiol60:765–782 [CrossRef][PubMed]
    [Google Scholar]
  10. Butcher B. G., Bronstein P. A., Myers C. R., Stodghill P. V., Bolton J. J., Markel E. J., Filiatrault M. J., Swingle B., Gaballa A.. & other authors ( 2011;). Characterization of the Fur regulon in Pseudomonas syringae pv. tomato DC3000. J Bacteriol193:4598–4611 [CrossRef][PubMed]
    [Google Scholar]
  11. Caswell C. C., Gaines J. M., Ciborowski P., Smith D., Borchers C. H., Roux C. M., Sayood K., Dunman P. M., Roop Ii R. M. II. ( 2012;). Identification of two small regulatory RNAs linked to virulence in Brucella abortus 2308. Mol Microbiol85:345–360 [CrossRef][PubMed]
    [Google Scholar]
  12. Chao Y., Vogel J.. ( 2010;). The role of Hfq in bacterial pathogens. Curr Opin Microbiol13:24–33 [CrossRef][PubMed]
    [Google Scholar]
  13. Chatterjee A., Cui Y., Yang H., Collmer A., Alfano J. R., Chatterjee A. K.. ( 2003;). GacA, the response regulator of a two-component system, acts as a master regulator in Pseudomonas syringae pv. tomato DC3000 by controlling regulatory RNA, transcriptional activators, and alternate sigma factors. Mol Plant Microbe Interact16:1106–1117 [CrossRef][PubMed]
    [Google Scholar]
  14. Christiansen J. K., Larsen M. H., Ingmer H., Søgaard-Andersen L., Kallipolitis B. H.. ( 2004;). The RNA-binding protein Hfq of Listeria monocytogenes: role in stress tolerance and virulence. J Bacteriol186:3355–3362 [CrossRef][PubMed]
    [Google Scholar]
  15. De Lay N., Gottesman S.. ( 2012;). A complex network of small non-coding RNAs regulate motility in Escherichia coli . Mol Microbiol86:524–538 [CrossRef][PubMed]
    [Google Scholar]
  16. Ding Y., Davis B. M., Waldor M. K.. ( 2004;). Hfq is essential for Vibrio cholerae virulence and downregulates sigma expression. Mol Microbiol53:345–354 [CrossRef][PubMed]
    [Google Scholar]
  17. Dong X., Mindrinos M., Davis K. R., Ausubel F. M.. ( 1991;). Induction of Arabidopsis defense genes by virulent and avirulent Pseudomonas syringae strains and by a cloned avirulence gene. Plant Cell3:61–72[PubMed][CrossRef]
    [Google Scholar]
  18. Filiatrault M. J., Stodghill P. V., Bronstein P. A., Moll S., Lindeberg M., Grills G., Schweitzer P., Wang W., Schroth G. P.. & other authors ( 2010;). Transcriptome analysis of Pseudomonas syringae identifies new genes, noncoding RNAs, and antisense activity. J Bacteriol192:2359–2372 [CrossRef][PubMed]
    [Google Scholar]
  19. Filiatrault M. J., Stodghill P. V., Myers C. R., Bronstein P. A., Butcher B. G., Lam H., Grills G., Schweitzer P., Wang W.. & other authors ( 2011;). Genome-wide identification of transcriptional start sites in the plant pathogen Pseudomonas syringae pv. tomato str. DC3000. PLoS ONE6:e29335 [CrossRef][PubMed]
    [Google Scholar]
  20. Geng J., Song Y., Yang L., Feng Y., Qiu Y., Li G., Guo J., Bi Y., Qu Y.. & other authors ( 2009;). Involvement of the post-transcriptional regulator Hfq in Yersinia pestis virulence. PLoS ONE4:e6213 [CrossRef][PubMed]
    [Google Scholar]
  21. González N., Heeb S., Valverde C., Kay E., Reimmann C., Junier T., Haas D.. ( 2008;). Genome-wide search reveals a novel GacA-regulated small RNA in Pseudomonas species. BMC Genomics9:167 [CrossRef][PubMed]
    [Google Scholar]
  22. Gottesman S.. ( 2005;). Micros for microbes: non-coding regulatory RNAs in bacteria. Trends Genet21:399–404 [CrossRef][PubMed]
    [Google Scholar]
  23. Gottesman S., McCullen C. A., Guillier M., Vanderpool C. K., Majdalani N., Benhammou J., Thompson K. M., FitzGerald P. C., Sowa N. A., FitzGerald D. J.. ( 2006;). Small RNA regulators and the bacterial response to stress. Cold Spring Harb Symp Quant Biol71:1–11 [CrossRef][PubMed]
    [Google Scholar]
  24. Hagen M. J., Stockwell V. O., Whistler C. A., Johnson K. B., Loper J. E.. ( 2009;). Stress tolerance and environmental fitness of Pseudomonas fluorescens A506, which has a mutation in RpoS. Phytopathology99:679–688 [CrossRef][PubMed]
    [Google Scholar]
  25. Hanahan D.. ( 1983;). Studies on transformation of Escherichia coli with plasmids. J Mol Biol166:557–580 [CrossRef][PubMed]
    [Google Scholar]
  26. Hébrard M., Kröger C., Srikumar S., Colgan A., Händler K., Hinton J. C.. ( 2012;). sRNAs and the virulence of Salmonella enterica serovar Typhimurium. RNA Biol9:437–445 [CrossRef][PubMed]
    [Google Scholar]
  27. Heeb S., Valverde C., Gigot-Bonnefoy C., Haas D.. ( 2005;). Role of the stress sigma factor RpoS in GacA/RsmA-controlled secondary metabolism and resistance to oxidative stress in Pseudomonas fluorescens CHA0. FEMS Microbiol Lett243:251–258 [CrossRef][PubMed]
    [Google Scholar]
  28. Heurlier K., Williams F., Heeb S., Dormond C., Pessi G., Singer D., Cámara M., Williams P., Haas D.. ( 2004;). Positive control of swarming, rhamnolipid synthesis, and lipase production by the posttranscriptional RsmA/RsmZ system in Pseudomonas aeruginosa PAO1. J Bacteriol186:2936–2945 [CrossRef][PubMed]
    [Google Scholar]
  29. Humair B., González N., Mossialos D., Reimmann C., Haas D.. ( 2009;). Temperature-responsive sensing regulates biocontrol factor expression in Pseudomonas fluorescens CHA0. ISME J3:955–965 [CrossRef][PubMed]
    [Google Scholar]
  30. Ishiga Y., Ishiga T., Uppalapati S. R., Mysore K. S.. ( 2011;). Arabidopsis seedling flood-inoculation technique: a rapid and reliable assay for studying plant-bacterial interactions. Plant Methods7:32 [CrossRef][PubMed]
    [Google Scholar]
  31. Jørgensen F., Bally M., Chapon-Herve V., Michel G., Lazdunski A., Williams P., Stewart G. S.. ( 1999;). RpoS-dependent stress tolerance in Pseudomonas aeruginosa . Microbiology145:835–844 [CrossRef][PubMed]
    [Google Scholar]
  32. Kidambi S. P., Sundin G. W., Palmer D. A., Chakrabarty A. M., Bender C. L.. ( 1995;). Copper as a signal for alginate synthesis in Pseudomonas syringae pv. syringae . Appl Environ Microbiol61:2172–2179[PubMed]
    [Google Scholar]
  33. King E. O., Ward M. K., Raney D. E.. ( 1954;). Two simple media for the demonstration of pyocyanin and fluorescin. J Lab Clin Med44:301–307[PubMed]
    [Google Scholar]
  34. Kreikemeyer B., Boyle M. D., Buttaro B. A., Heinemann M., Podbielski A.. ( 2001;). Group A streptococcal growth phase-associated virulence factor regulation by a novel operon (Fas) with homologies to two-component-type regulators requires a small RNA molecule. Mol Microbiol39:392–406 [CrossRef][PubMed]
    [Google Scholar]
  35. Le Rhun A., Charpentier E.. ( 2012;). Small RNAs in streptococci. RNA Biol9:414–426 [CrossRef][PubMed]
    [Google Scholar]
  36. Lenz D. H., Mok K. C., Lilley B. N., Kulkarni R. V., Wingreen N. S., Bassler B. L.. ( 2004;). The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae . Cell118:69–82 [CrossRef][PubMed]
    [Google Scholar]
  37. Lenz D. H., Miller M. B., Zhu J., Kulkarni R. V., Bassler B. L.. ( 2005;). CsrA and three redundant small RNAs regulate quorum sensing in Vibrio cholerae . Mol Microbiol58:1186–1202 [CrossRef][PubMed]
    [Google Scholar]
  38. Levine A., Tenhaken R., Dixon R., Lamb C.. ( 1994;). H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell79:583–593 [CrossRef][PubMed]
    [Google Scholar]
  39. Liu Y., Wu N., Dong J., Gao Y., Zhang X., Mu C., Shao N., Yang G.. ( 2010;). Hfq is a global regulator that controls the pathogenicity of Staphylococcus aureus . PLoS ONE5:5[PubMed]
    [Google Scholar]
  40. Livny J., Brencic A., Lory S., Waldor M. K.. ( 2006;). Identification of 17 Pseudomonas aeruginosa sRNAs and prediction of sRNA-encoding genes in 10 diverse pathogens using the bioinformatic tool sRNAPredict2. Nucleic Acids Res34:3484–3493 [CrossRef][PubMed]
    [Google Scholar]
  41. López D., Kolter R.. ( 2010;). Functional microdomains in bacterial membranes. Genes Dev24:1893–1902 [CrossRef][PubMed]
    [Google Scholar]
  42. Majdalani N., Vanderpool C. K., Gottesman S.. ( 2005;). Bacterial small RNA regulators. Crit Rev Biochem Mol Biol40:93–113 [CrossRef][PubMed]
    [Google Scholar]
  43. Mangold M., Siller M., Roppenser B., Vlaminckx B. J., Penfound T. A., Klein R., Novak R., Novick R. P., Charpentier E.. ( 2004;). Synthesis of group A streptococcal virulence factors is controlled by a regulatory RNA molecule. Mol Microbiol53:1515–1527 [CrossRef][PubMed]
    [Google Scholar]
  44. Markel E., Maciak C., Butcher B. G., Myers C. R., Stodghill P., Bao Z., Cartinhour S., Swingle B.. ( 2011;). An extracytoplasmic function sigma factor-mediated cell surface signaling system in Pseudomonas syringae pv. tomato DC3000 regulates gene expression in response to heterologous siderophores. J Bacteriol193:5775–5783 [CrossRef][PubMed]
    [Google Scholar]
  45. Massé E., Salvail H., Desnoyers G., Arguin M.. ( 2007;). Small RNAs controlling iron metabolism. Curr Opin Microbiol10:140–145 [CrossRef][PubMed]
    [Google Scholar]
  46. Miguel E., Poza-Carrión C., López-Solanilla E., Aguilar I., Llama-Palacios A., García-Olmedo F., Rodríguez-Palenzuela P.. ( 2000;). Evidence against a direct antimicrobial role of H2O2 in the infection of plants by Erwinia chrysanthemi . Mol Plant Microbe Interact13:421–429 [CrossRef][PubMed]
    [Google Scholar]
  47. Miller C. D., Mortensen W. S., Braga G. U., Anderson A. J.. ( 2001;). The rpoS gene in Pseudomonas syringae is important in surviving exposure to the near-UV in sunlight. Curr Microbiol43:374–377 [CrossRef][PubMed]
    [Google Scholar]
  48. Palmer D. A., Bender C. L.. ( 1993;). Effects of environmental and nutritional factors on production of the polyketide phytotoxin coronatine by Pseudomonas syringae pv. glycinea . Appl Environ Microbiol59:1619–1626[PubMed]
    [Google Scholar]
  49. Péchy-Tarr M., Bottiglieri M., Mathys S., Lejbølle K. B., Schnider-Keel U., Maurhofer M., Keel C.. ( 2005;). RpoN (σ54) controls production of antifungal compounds and biocontrol activity in Pseudomonas fluorescens CHA0. Mol Plant Microbe Interact18:260–272 [CrossRef][PubMed]
    [Google Scholar]
  50. Pressler U., Staudenmaier H., Zimmermann L., Braun V.. ( 1988;). Genetics of the iron dicitrate transport system of Escherichia coli . J Bacteriol170:2716–2724[PubMed]
    [Google Scholar]
  51. Romby P., Vandenesch F., Wagner E. G.. ( 2006;). The role of RNAs in the regulation of virulence-gene expression. Curr Opin Microbiol9:229–236 [CrossRef][PubMed]
    [Google Scholar]
  52. Schäfer A., Tauch A., Jäger W., Kalinowski J., Thierbach G., Pühler A.. ( 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 . Gene145:69–73 [CrossRef][PubMed]
    [Google Scholar]
  53. Schagat T., Paguio A., Kopish K.. ( 2007;). Normalizing genetic reporter assays: approaches and considerations for increasing consistency and statistical significance. Cell Notes17:9–12
    [Google Scholar]
  54. Schurr M. J., Yu H., Boucher J. C., Hibler N. S., Deretic V.. ( 1995;). Multiple promoters and induction by heat shock of the gene encoding the alternative sigma factor AlgU (σE) which controls mucoidy in cystic fibrosis isolates of Pseudomonas aeruginosa . J Bacteriol177:5670–5679[PubMed]
    [Google Scholar]
  55. Silvaggi J. M., Perkins J. B., Losick R.. ( 2006;). Genes for small, noncoding RNAs under sporulation control in Bacillus subtilis . J Bacteriol188:532–541 [CrossRef][PubMed]
    [Google Scholar]
  56. Sonnleitner E., Hagens S., Rosenau F., Wilhelm S., Habel A., Jäger K. E., Bläsi U.. ( 2003;). Reduced virulence of a hfq mutant of Pseudomonas aeruginosa O1. Microb Pathog35:217–228 [CrossRef][PubMed]
    [Google Scholar]
  57. Sonnleitner E., Romeo A., Bläsi U.. ( 2012;). Small regulatory RNAs in Pseudomonas aeruginosa . RNA Biol9:364–371 [CrossRef][PubMed]
    [Google Scholar]
  58. Stockwell V. O., Loper J. E.. ( 2005;). The sigma factor RpoS is required for stress tolerance and environmental fitness of Pseudomonas fluorescens Pf-5. Microbiology151:3001–3009 [CrossRef][PubMed]
    [Google Scholar]
  59. Stockwell V. O., Hockett K., Loper J. E.. ( 2009;). Role of RpoS in stress tolerance and environmental fitness of the phyllosphere bacterium Pseudomonas fluorescens strain 122. Phytopathology99:689–695 [CrossRef][PubMed]
    [Google Scholar]
  60. Suh S. J., Silo-Suh L., Woods D. E., Hassett D. J., West S. E., Ohman D. E.. ( 1999;). Effect of rpoS mutation on the stress response and expression of virulence factors in Pseudomonas aeruginosa . J Bacteriol181:3890–3897[PubMed]
    [Google Scholar]
  61. Swingle B., Thete D., Moll M., Myers C. R., Schneider D. J., Cartinhour S.. ( 2008;). Characterization of the PvdS-regulated promoter motif in Pseudomonas syringae pv. tomato DC3000 reveals regulon members and insights regarding PvdS function in other pseudomonads. Mol Microbiol68:871–889 [CrossRef][PubMed]
    [Google Scholar]
  62. Torres-Quesada O., Oruezabal R. I., Peregrina A., Jofré E., Lloret J., Rivilla R., Toro N., Jiménez-Zurdo J. I.. ( 2010;). The Sinorhizobium meliloti RNA chaperone Hfq influences central carbon metabolism and the symbiotic interaction with alfalfa. BMC Microbiol10:71 [CrossRef][PubMed]
    [Google Scholar]
  63. Vencato M., Tian F., Alfano J. R., Buell C. R., Cartinhour S., DeClerck G. A., Guttman D. S., Stavrinides J., Joardar V.. & other authors ( 2006;). Bioinformatics-enabled identification of the HrpL regulon and type III secretion system effector proteins of Pseudomonas syringae pv. phaseolicola 1448A. Mol Plant Microbe Interact19:1193–1206 [CrossRef][PubMed]
    [Google Scholar]
  64. Vogel J., Luisi B. F.. ( 2011;). Hfq and its constellation of RNA. Nat Rev Microbiol9:578–589 [CrossRef][PubMed]
    [Google Scholar]
  65. Windgassen M., Urban A., Jaeger K. E.. ( 2000;). Rapid gene inactivation in Pseudomonas aeruginosa . FEMS Microbiol Lett193:201–205 [CrossRef][PubMed]
    [Google Scholar]
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