Skip to main content
PMC home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1996 Sep 3;93(18):9839–9843. doi: 10.1073/pnas.93.18.9839

The alginate regulator AlgR and an associated sensor FimS are required for twitching motility in Pseudomonas aeruginosa.

C B Whitchurch 1, R A Alm 1, J S Mattick 1
PMCID: PMC38516  PMID: 8790418

Abstract

Mucoid strains of Pseudomonas aeruginosa isolated from the lungs of cystic fibrosis patients produce large amounts of the exopolysaccharide alginate. AlgR has long been considered a key regulator of alginate production, but its cognate sensor has not been identified. Here we show that AlgR is required for twitching motility, which is a form of bacterial surface translocation mediated by type 4 fimbriae. Adjacent to algR we have identified a sensor gene (fimS), which is also required for twitching motility. However, FimS does not appear to be required for alginate production in mucoid strains. FimS and AlgR are representative of a new subclass of two-component transmitter-receiver regulatory systems. The alternative sigma factor AlgU also affects both alginate production and twitching motility. Therefore, these two virulence determinants appear to be closely associated and coordinately regulated.

Full text

PDF
9843

Images in this article

9840Fig. 1
on p.9840
9841Fig. 2
on p.9841
9842Fig. 3
on p.9842

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Alm R. A., Bodero A. J., Free P. D., Mattick J. S. Identification of a novel gene, pilZ, essential for type 4 fimbrial biogenesis in Pseudomonas aeruginosa. J Bacteriol. 1996 Jan;178(1):46–53. doi: 10.1128/jb.178.1.46-53.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Alm R. A., Mattick J. S. Identification of a gene, pilV, required for type 4 fimbrial biogenesis in Pseudomonas aeruginosa, whose product possesses a pre-pilin-like leader sequence. Mol Microbiol. 1995 May;16(3):485–496. doi: 10.1111/j.1365-2958.1995.tb02413.x. [DOI] [PubMed] [Google Scholar]
  3. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
  4. Bradley D. E. A function of Pseudomonas aeruginosa PAO polar pili: twitching motility. Can J Microbiol. 1980 Feb;26(2):146–154. doi: 10.1139/m80-022. [DOI] [PubMed] [Google Scholar]
  5. Brunskill E. W., Bayles K. W. Identification and molecular characterization of a putative regulatory locus that affects autolysis in Staphylococcus aureus. J Bacteriol. 1996 Feb;178(3):611–618. doi: 10.1128/jb.178.3.611-618.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Darzins A., Chakrabarty A. M. Cloning of genes controlling alginate biosynthesis from a mucoid cystic fibrosis isolate of Pseudomonas aeruginosa. J Bacteriol. 1984 Jul;159(1):9–18. doi: 10.1128/jb.159.1.9-18.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Deretic V., Dikshit R., Konyecsni W. M., Chakrabarty A. M., Misra T. K. The algR gene, which regulates mucoidy in Pseudomonas aeruginosa, belongs to a class of environmentally responsive genes. J Bacteriol. 1989 Mar;171(3):1278–1283. doi: 10.1128/jb.171.3.1278-1283.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Deretic V., Konyecsni W. M. Control of mucoidy in Pseudomonas aeruginosa: transcriptional regulation of algR and identification of the second regulatory gene, algQ. J Bacteriol. 1989 Jul;171(7):3680–3688. doi: 10.1128/jb.171.7.3680-3688.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Deretic V., Leveau J. H., Mohr C. D., Hibler N. S. In vitro phosphorylation of AlgR, a regulator of mucoidy in Pseudomonas aeruginosa, by a histidine protein kinase and effects of small phospho-donor molecules. Mol Microbiol. 1992 Oct;6(19):2761–2767. doi: 10.1111/j.1365-2958.1992.tb01455.x. [DOI] [PubMed] [Google Scholar]
  10. Deretic V., Schurr M. J., Boucher J. C., Martin D. W. Conversion of Pseudomonas aeruginosa to mucoidy in cystic fibrosis: environmental stress and regulation of bacterial virulence by alternative sigma factors. J Bacteriol. 1994 May;176(10):2773–2780. doi: 10.1128/jb.176.10.2773-2780.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Doig P., Todd T., Sastry P. A., Lee K. K., Hodges R. S., Paranchych W., Irvin R. T. Role of pili in adhesion of Pseudomonas aeruginosa to human respiratory epithelial cells. Infect Immun. 1988 Jun;56(6):1641–1646. doi: 10.1128/iai.56.6.1641-1646.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fyfe J. A., Govan J. R. Alginate synthesis in mucoid Pseudomonas aeruginosa: a chromosomal locus involved in control. J Gen Microbiol. 1980 Aug;119(2):443–450. doi: 10.1099/00221287-119-2-443. [DOI] [PubMed] [Google Scholar]
  13. Goldberg J. B., Gorman W. L., Flynn J. L., Ohman D. E. A mutation in algN permits trans activation of alginate production by algT in Pseudomonas species. J Bacteriol. 1993 Mar;175(5):1303–1308. doi: 10.1128/jb.175.5.1303-1308.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hazlett L. D., Moon M. M., Singh A., Berk R. S., Rudner X. L. Analysis of adhesion, piliation, protease production and ocular infectivity of several P. aeruginosa strains. Curr Eye Res. 1991 Apr;10(4):351–362. doi: 10.3109/02713689108996341. [DOI] [PubMed] [Google Scholar]
  15. Higgins D. G., Sharp P. M. Fast and sensitive multiple sequence alignments on a microcomputer. Comput Appl Biosci. 1989 Apr;5(2):151–153. doi: 10.1093/bioinformatics/5.2.151. [DOI] [PubMed] [Google Scholar]
  16. Hobbs M., Collie E. S., Free P. D., Livingston S. P., Mattick J. S. PilS and PilR, a two-component transcriptional regulatory system controlling expression of type 4 fimbriae in Pseudomonas aeruginosa. Mol Microbiol. 1993 Mar;7(5):669–682. doi: 10.1111/j.1365-2958.1993.tb01158.x. [DOI] [PubMed] [Google Scholar]
  17. Hobbs M., Mattick J. S. Common components in the assembly of type 4 fimbriae, DNA transfer systems, filamentous phage and protein-secretion apparatus: a general system for the formation of surface-associated protein complexes. Mol Microbiol. 1993 Oct;10(2):233–243. doi: 10.1111/j.1365-2958.1993.tb01949.x. [DOI] [PubMed] [Google Scholar]
  18. Kimbara K., Chakrabarty A. M. Control of alginate synthesis in Pseudomonas aeruginosa: regulation of the algR1 gene. Biochem Biophys Res Commun. 1989 Oct 31;164(2):601–608. doi: 10.1016/0006-291x(89)91502-7. [DOI] [PubMed] [Google Scholar]
  19. Mattick J. S., Bills M. M., Anderson B. J., Dalrymple B., Mott M. R., Egerton J. R. Morphogenetic expression of Bacteroides nodosus fimbriae in Pseudomonas aeruginosa. J Bacteriol. 1987 Jan;169(1):33–41. doi: 10.1128/jb.169.1.33-41.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. May T. B., Chakrabarty A. M. Isolation and assay of Pseudomonas aeruginosa alginate. Methods Enzymol. 1994;235:295–304. doi: 10.1016/0076-6879(94)35148-1. [DOI] [PubMed] [Google Scholar]
  21. Mohr C. D., Deretic V. Gene-scrambling mutagenesis: generation and analysis of insertional mutations in the alginate regulatory region of Pseudomonas aeruginosa. J Bacteriol. 1990 Nov;172(11):6252–6260. doi: 10.1128/jb.172.11.6252-6260.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Mohr C. D., Martin D. W., Konyecsni W. M., Govan J. R., Lory S., Deretic V. Role of the far-upstream sites of the algD promoter and the algR and rpoN genes in environmental modulation of mucoidy in Pseudomonas aeruginosa. J Bacteriol. 1990 Nov;172(11):6576–6580. doi: 10.1128/jb.172.11.6576-6580.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Mohr C. D., Sonsteby S. K., Deretic V. The Pseudomonas aeruginosa homologs of hemC and hemD are linked to the gene encoding the regulator of mucoidy AlgR. Mol Gen Genet. 1994 Jan;242(2):177–184. doi: 10.1007/BF00391011. [DOI] [PubMed] [Google Scholar]
  24. Pao G. M., Saier M. H., Jr Response regulators of bacterial signal transduction systems: selective domain shuffling during evolution. J Mol Evol. 1995 Feb;40(2):136–154. doi: 10.1007/BF00167109. [DOI] [PubMed] [Google Scholar]
  25. Parkinson J. S., Kofoid E. C. Communication modules in bacterial signaling proteins. Annu Rev Genet. 1992;26:71–112. doi: 10.1146/annurev.ge.26.120192.000443. [DOI] [PubMed] [Google Scholar]
  26. Parkinson J. S. Signal transduction schemes of bacteria. Cell. 1993 Jun 4;73(5):857–871. doi: 10.1016/0092-8674(93)90267-t. [DOI] [PubMed] [Google Scholar]
  27. Shimkets L. J. Social and developmental biology of the myxobacteria. Microbiol Rev. 1990 Dec;54(4):473–501. doi: 10.1128/mr.54.4.473-501.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Simon R., Quandt J., Klipp W. New derivatives of transposon Tn5 suitable for mobilization of replicons, generation of operon fusions and induction of genes in gram-negative bacteria. Gene. 1989 Aug 1;80(1):161–169. doi: 10.1016/0378-1119(89)90262-x. [DOI] [PubMed] [Google Scholar]
  29. Swanson R. V., Alex L. A., Simon M. I. Histidine and aspartate phosphorylation: two-component systems and the limits of homology. Trends Biochem Sci. 1994 Nov;19(11):485–490. doi: 10.1016/0968-0004(94)90135-x. [DOI] [PubMed] [Google Scholar]
  30. Watson A. A., Alm R. A., Mattick J. S. Construction of improved vectors for protein production in Pseudomonas aeruginosa. Gene. 1996 Jun 12;172(1):163–164. doi: 10.1016/0378-1119(96)00026-1. [DOI] [PubMed] [Google Scholar]
  31. Wu S. S., Kaiser D. Genetic and functional evidence that Type IV pili are required for social gliding motility in Myxococcus xanthus. Mol Microbiol. 1995 Nov;18(3):547–558. doi: 10.1111/j.1365-2958.1995.mmi_18030547.x. [DOI] [PubMed] [Google Scholar]
  32. Zielinski N. A., Roychoudhury S., Chakrabarty A. M. Regulation of alginate gene expression in Pseudomonas aeruginosa. Methods Enzymol. 1994;235:493–502. doi: 10.1016/0076-6879(94)35165-1. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES