Pseudomonas aeruginosa biofilm matrix polysaccharide Psl is regulated transcriptionally by RpoS and post‐transcriptionally by RsmA

Abstract

Summary Extracellular polysaccharides are important components of biofilms. In non‐mucoid Pseudomonas aeruginosa strains, the Pel and Psl polysaccharides are major structural components of the biofilm matrix. In this study, we demonstrate that the alternative σ‐factor RpoS is a positive transcriptional regulator of psl gene expression. Furthermore, we show that psl mRNA has an extensive 5′ untranslated region, to which the post‐transcriptional regulator RsmA binds and represses psl translation. Our observations suggest that upon binding RsmA, the region spanning the ribosome binding site of psl mRNA folds into a secondary stem‐loop structure that blocks the Shine–Dalgarno sequence, preventing ribosome access and protein translation. This constitutes a novel mechanism for translational repression by this family of regulators.

Shown for reading. Its publisher allows quoting it, not republishing it.

References 69

1. 1.

   Adams JL, McLean RJ. Impact of rpoS deletion on Escherichia coli biofilms. Appl Environ Microbiol. 1999;65:4285-4287.

   Not in our library10.1128/aem.65.9.4285-4287.1999

2. 2.

   Babitzke P, Baker CS, Romeo T. Regulation of translation initiation by RNA binding proteins. Annu Rev Microbiol. 2009;63:27-44.

   Not in our library10.1146/annurev.micro.091208.073514

3. 3.

   Baker CS, Morozov I, Suzuki K, Romeo T, Babitzke P. CsrA regulates glycogen biosynthesis by preventing translation of glgC in Escherichia coli. Mol Microbiol. 2002;44:1599-1610.

   Not in our library10.1046/j.1365-2958.2002.02982.x

4. 4.

   Baker CS, Eöry LA, Yakhnin H, Mercante J, Romeo T, Babitzke P. CsrA inhibits translation initiation of Escherichia coli hfq by binding to a single site overlapping the Shine–Dalgarno sequence. J Bacteriol. 2007;189:5472-5481.

   Not in our library10.1128/jb.00529-07

5. 5.

   Barne KA, Bown JA, Busby SJ, Minchin SD. Region 2.5 of the Escherichia coli RNA polymerase σ70 subunit is responsible for the recognition of the ‘extended–10’ motif at promoters. EMBO J. 1997;16:4034-4040.

   Not in our library10.1093/emboj/16.13.4034

6. 6.
   Pseudomonas aeruginosa uses a cyclic‐di‐GMP‐regulated adhesin to reinforce the biofilm extracellular matrix · 2010

   No notice
7. 7.

   Branda SS, Vik S, Friedman L, Kolter R. Biofilms: the matrix revisited. Trends Microbiol. 2005;13:20-26.

   Not in our library10.1016/j.tim.2004.11.006

8. 8.

   Brencic A, Lory S. Determination of the regulon and identification of novel mRNA targets of Pseudomonas aeruginosa RsmA. Mol Microbiol. 2009;72:612-632.

   Not in our library10.1111/j.1365-2958.2009.06670.x

9. 9.

   Burrowes E, Baysse C, Adams C, O'Gara F. Influence of the regulatory protein RsmA on cellular functions in Pseudomonas aeruginosa PAO1, as revealed by transcriptome analysis. Microbiology. 2006;152:405-418.

   Not in our library10.1099/mic.0.28324-0

10. 10.

    Byrd MS, Sadovskaya I, Vinogradov E, Lu H, Sprinkle AB, Richardson SH, et al. Genetic and biochemical analyses of the Pseudomonas aeruginosa Psl exopolysaccharide reveal overlapping roles for polysaccharide synthesis enzymes in Psl and LPS production. Mol Microbiol. 2009;73:622-638.

    Not in our library10.1111/j.1365-2958.2009.06795.x

11. 11.

    Chavez RG, Alvarez AF, Romeo T, Georgellis D. The physiological stimulus for the BarA sensor kinase. J Bacteriol. 2010;192:2009-2012.

    Not in our library10.1128/jb.01685-09

12. 12.

    Choi KH, Kumar A, Schweizer HP. 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. 2006;64:391-397.

    Not in our library10.1016/j.mimet.2005.06.001

13. 13.

    Corona-Izquierdo FP, Membrillo-Hernández J. A mutation in rpoS enhances biofilm formation in Escherichia coli during exponential phase of growth. FEMS Microbiol Lett. 2002;211:105-110.

    Not in our library10.1111/j.1574-6968.2002.tb11210.x

14. 14.

    Drenkard E, Ausubel FM. Pseudomonas biofilm formation and antibiotic resistance are linked to phenotypic variation. Nature. 2002;416:740-743.

    Not in our library10.1038/416740a

15. 15.

    Dubey AK, Baker CS, Suzuki K, Jones AD, Pandit P, Romeo T, Babitzke P. CsrA regulates translation of the Escherichia coli carbon starvation gene, cstA, by blocking ribosome access to the cstA transcript. J Bacteriol. 2003;185:4450-4460.

    Not in our library10.1128/jb.185.15.4450-4460.2003

16. 16.

    Dubey AK, Baker CS, Romeo T, Babitzke P. RNA sequence and secondary structure participate in high-affinity CsrA-RNA interaction. RNA. 2005;11:1579-1587.

    Not in our library10.1261/rna.2990205

17. 17.

    Friedman L, Kolter R. Two genetic loci produce distinct carbohydrate-rich structural components of the Pseudomonas aeruginosa biofilm matrix. J Bacteriol. 2004;186:4457-4465.

    Not in our library10.1128/jb.186.14.4457-4465.2004

18. 18.

    Gilbert KB, Kim TH, Gupta R, Greenberg EP, Schuster M. Global position analysis of the Pseudomonas aeruginosa quorum-sensing transcription factor LasR. Mol Microbiol. 2009;73:1072-1085.

    Not in our library10.1111/j.1365-2958.2009.06832.x

19. 19.

    Govan JR, Deretic V. Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia. Microbiol Rev. 1996;60:539-574.

    Not in our library10.1128/mr.60.3.539-574.1996

20. 20.

    Gudapaty S, Suzuki K, Wang X, Babitzke P, Romeo T. Regulatory interactions of Csr components: the RNA binding protein CsrA activates csrB transcription in Escherichia coli. J Bacteriol. 2001;183:6017-6027.

    Not in our library10.1128/jb.183.20.6017-6027.2001

21. 21.

    Gutiérrez P, Li Y, Osborne MJ, Pomerantseva E, Liu Q, Gehring K. Solution structure of the carbon storage regulator protein CsrA from Escherichia coli. J Bacteriol. 2005;187:3496-3501.

    Not in our library10.1128/jb.187.10.3496-3501.2005

22. 22.

    Güvener ZT, Harwood CS. Subcellular location characteristics of the Pseudomonas aeruginosa GGDEF protein, WspR, indicate that it produces cyclic-di-GMP in response to growth on surfaces. Mol Microbiol. 2007;66:1459-1473.

    Not in our library10.1111/j.1365-2958.2007.06008.x

23. 23.

    Hentzer M, Teitzel GM, Balzer GJ, Heydorn A, Molin S, Givskov M, Parsek MR. Alginate overproduction affects Pseudomonas aeruginosa biofilm structure and function. J Bacteriol. 2001;183:5395-5401.

    Not in our library10.1128/jb.183.18.5395-5401.2001

24. 24.

    Heurlier K, Williams F, Heeb S, Dormond C, Pessi G, Singer D, et al. Positive control of swarming, rhamnolipid synthesis, and lipase production by the posttranscriptional RsmA/RsmZ system in Pseudomonas aeruginosa PAO1. J Bacteriol. 2004;186:2936-2945.

    Not in our library10.1128/jb.186.10.2936-2945.2004

25. 25.

    Hickman JW, Harwood CS. Identification of FleQ from Pseudomonas aeruginosa as a c-di-GMP-responsive transcription factor. Mol Microbiol. 2008;69:376-389.

    Not in our library10.1111/j.1365-2958.2008.06281.x

26. 26.

    Hickman JW, Tifrea DF, Harwood CS. A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels. Proc Natl Acad Sci USA. 2005;102:14422-14427.

    Not in our library10.1073/pnas.0507170102

27. 27.

    Hoang TT, Schweizer HP. Fatty acid biosynthesis in Pseudomonas aeruginosa: cloning and characterization of the fabAB operon encoding β-hydroxyacyl-acyl carrier protein dehydratase (FabA) and β-ketoacyl-acyl carrier protein synthase I (FabB). J Bacteriol. 1997;179:5326-5332.

    Not in our library10.1128/jb.179.17.5326-5332.1997

28. 28.

    Hoang TT, Karkhoff-Schweizer RR, Kutchma AJ, Schweizer HP. A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene. 1998;212:77-86.

    Not in our library10.1016/s0378-1119(98)00130-9

29. 29.

    Hoang TT, Kutchma AJ, Becher A, Schweizer HP. Integration-proficient plasmids for Pseudomonas aeruginosa: site-specific integration and use for engineering of reporter and expression strains. Plasmid. 2000;43:59-72.

    Not in our library10.1006/plas.1999.1441

30. 30.

    Humair B, Wackwitz B, Haas D. GacA-controlled activation of promoters for small RNA genes in Pseudomonas fluorescens. Appl Environ Microbiol. 2010;76:1497-1506.

    Not in our library10.1128/aem.02014-09

31. 31.

    Itoh Y, Rice JD, Goller C, Pannuri A, Taylor J, Meisner J, et al. Roles of pgaABCD genes in synthesis, modification, and export of the Escherichia coli biofilm adhesin poly-β-1,6-N-acetyl-D-glucosamine. J Bacteriol. 2008;190:3670-3680.

    Not in our library10.1128/jb.01920-07

32. 32.

    Jackson KD, Starkey M, Kremer S, Parsek MR, Wozniak DJ. Identification of psl, a locus encoding a potential exopolysaccharide that is essential for Pseudomonas aeruginosa PAO1 biofilm formation. J Bacteriol. 2004;186:4466-4475.

    Not in our library10.1128/jb.186.14.4466-4475.2004

33. 33.

    Jonas K, Edwards AN, Ahmad I, Romeo T, Römling U, Melefors Ö. Complex regulatory network encompassing the Csr, c-di-GMP and motility systems of Salmonella Typhimurium. Environ Microbiol. 2009;12:524-540.

    Not in our library10.1111/j.1462-2920.2009.02097.x

34. 34.

    Kirisits MJ, Prost L, Starkey M, Parsek MR. Characterization of colony morphology variants isolated from Pseudomonas aeruginosa biofilms. Appl Environ Microbiol. 2005;71:4809-4821.

    Not in our library10.1128/aem.71.8.4809-4821.2005

35. 35.

    Lapouge K, Sineva E, Lindell M, Starke K, Baker CS, Babitzke P, Haas D. Mechanism of hcnA mRNA recognition in the Gac/Rsm signal transduction pathway of Pseudomonas fluorescens. Mol Microbiol. 2007;66:341-356.

    Not in our library10.1111/j.1365-2958.2007.05909.x

36. 36.

    Lapouge K, Schubert M, Allain FH, Haas D. Gac/Rsm signal transduction pathway of γ-proteobacteria: from RNA recognition to regulation of social behaviour. Mol Microbiol. 2008;67:241-253.

    Not in our library10.1111/j.1365-2958.2007.06042.x

37. 37.
    A cyclic‐di‐GMP receptor required for bacterial exopolysaccharide production · 2007

    No notice
38. 38.

    Lequette Y, Lee J-H, Ledgham F, Lazdunski A, Greenberg EP. A distinct QscR regulon in the Pseudomonas aeruginosa quorum-sensing circuit. J Bacteriol. 2006;188:3365-3370.

    Not in our library10.1128/jb.188.9.3365-3370.2006

39. 39.

    Liu MY, Gui G, Wei B, Preston JF, Oakford L, Yüksel Ü, et al. The RNA molecule CsrB binds to the global regulatory protein CsrA and antagonizes its activity in Escherichia coli. J Biol Chem. 1997;272:17502-17510.

    Not in our library10.1074/jbc.272.28.17502

40. 40.

    Ma L, Jackson KD, Landry RM, Parsek MR, Wozniak DJ. Analysis of Pseudomonas aeruginosa conditional psl variants reveals roles for the psl polysaccharide in adhesion and maintaining biofilm structure postattachment. J Bacteriol. 2006;188:8213-8221.

    Not in our library10.1128/jb.01202-06

Cited by papers we hold 8

• Biofilms by bacterial human pathogens: Clinical relevance - development, composition and regulation - therapeutical strategies · 2021
  No notice
• Anti-biofilm activity of plant derived extracts against infectious pathogen-Pseudomonas aeruginosa PAO1 · 2020
  Not checked
• Pseudomonas aeruginosa Lifestyle: A Paradigm for Adaptation, Survival, and Persistence · 2017
  No notice
• Matrix exopolysaccharides; the sticky side of biofilm formation · 2017
  No notice
• The Formation of Biofilms by Pseudomonas aeruginosa : A Review of the Natural and Synthetic Compounds Interfering with Control Mechanisms · 2015
  No notice
• RNA-binding proteins involved in post-transcriptional regulation in bacteria · 2015
  No notice
• Biofilm Matrix and Its Regulation in Pseudomonas aeruginosa · 2013
  No notice
• The Pseudomonas aeruginosa Reference Strain PA14 Displays Increased Virulence Due to a Mutation in ladS · 2011
  No notice

Reads

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.