Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1997 Jun;179(11):3711–3720. doi: 10.1128/jb.179.11.3711-3720.1997

Posttranslational control of the algT (algU)-encoded sigma22 for expression of the alginate regulon in Pseudomonas aeruginosa and localization of its antagonist proteins MucA and MucB (AlgN).

K Mathee 1, C J McPherson 1, D E Ohman 1
PMCID: PMC179169  PMID: 9171421

Abstract

Pseudomonas aeruginosa strains associated with cystic fibrosis are often mucoid due to the copious production of alginate, an exopolysaccharide and virulence factor. Alginate gene expression is transcriptionally controlled by a gene cluster at 68 min on the chromosome: algT (algU)-mucA-mucB (algN)-mucC (algM)-mucD (algY). The algT gene encodes a 22-kDa alternative sigma factor (sigma22) that autoregulates its own promoter (PalgT) as well as the promoters of algR, algB, and algD. The other genes in the algT cluster appear to regulate the expression or activity of sigma22. The goal of this study was to better understand the functional interactions between sigma22 and its antagonist regulators during alginate production. Nonmucoid strain PAO1 was made to overproduce alginate (indicating high algD promoter activity) through increasing sigma22 in the cell by introducing a plasmid clone containing algT from mucA22(Def) strain FRD1. However, the bacterial cells remained nonmucoid if the transcriptionally coupled mucB on the clone remained intact. This suggested that a stoichiometric relationship between sigma22 and MucB may be required to control sigma factor activity. When the transcription and translational initiation of algT were measured with lacZ fusions, alginate production correlated with only about a 1.2- to 1.7-fold increase in algT-lacZ activity, respectively. An algR-lacZ transcriptional fusion showed a 2.8-fold increase in transcription with alginate production under the same conditions. A Western blot analysis of total cell extracts showed that sigma22 was approximately 10-fold higher in strains that overproduced alginate, even though algT expression increased less than 2-fold. This suggested that a post-transcriptional mechanism may exist to destabilize sigma22 in order to control certain sigma22-dependent promoters like algD. By Western blotting and phoA fusion analyses, the MucB antagonist of sigma22 was found to localize to the periplasm of the cell. Similar experiments suggest that MucA localizes to the inner membrane via one transmembrane domain with amino- and carboxy-terminal domains in the cytoplasm and periplasm, respectively. These data were used to propose a model in which MucB-MucA-sigma22 interact via an inner membrane complex that controls the stability of sigma22 protein in order to control alginate biosynthesis.

Full Text

The Full Text of this article is available as a PDF (1.1 MB).

Selected References

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

  1. Baltimore R. S., Mitchell M. Immunologic investigations of mucoid strains of Pseudomonas aeruginosa: comparison of susceptibility to opsonic antibody in mucoid and nonmucoid strains. J Infect Dis. 1980 Feb;141(2):238–247. doi: 10.1093/infdis/141.2.238. [DOI] [PubMed] [Google Scholar]
  2. Boucher J. C., Martinez-Salazar J., Schurr M. J., Mudd M. H., Yu H., Deretic V. Two distinct loci affecting conversion to mucoidy in Pseudomonas aeruginosa in cystic fibrosis encode homologs of the serine protease HtrA. J Bacteriol. 1996 Jan;178(2):511–523. doi: 10.1128/jb.178.2.511-523.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Boyd A., Ghosh M., May T. B., Shinabarger D., Keogh R., Chakrabarty A. M. Sequence of the algL gene of Pseudomonas aeruginosa and purification of its alginate lyase product. Gene. 1993 Sep 6;131(1):1–8. doi: 10.1016/0378-1119(93)90662-m. [DOI] [PubMed] [Google Scholar]
  4. Cheng K. J., Ingram J. M., Costerton J. W. Interactions of alkaline phosphatase and the cell wall of Pseudomonas aeruginosa. J Bacteriol. 1971 Jul;107(1):325–336. doi: 10.1128/jb.107.1.325-336.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chi E., Bartlett D. H. An rpoE-like locus controls outer membrane protein synthesis and growth at cold temperatures and high pressures in the deep-sea bacterium Photobacterium sp. strain SS9. Mol Microbiol. 1995 Aug;17(4):713–726. doi: 10.1111/j.1365-2958.1995.mmi_17040713.x. [DOI] [PubMed] [Google Scholar]
  6. Chitnis C. E., Ohman D. E. Cloning of Pseudomonas aeruginosa algG, which controls alginate structure. J Bacteriol. 1990 Jun;172(6):2894–2900. doi: 10.1128/jb.172.6.2894-2900.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chitnis C. E., Ohman D. E. Genetic analysis of the alginate biosynthetic gene cluster of Pseudomonas aeruginosa shows evidence of an operonic structure. Mol Microbiol. 1993 May;8(3):583–593. doi: 10.1111/j.1365-2958.1993.tb01602.x. [DOI] [PubMed] [Google Scholar]
  8. Chu L., May T. B., Chakrabarty A. M., Misra T. K. Nucleotide sequence and expression of the algE gene involved in alginate biosynthesis by Pseudomonas aeruginosa. Gene. 1991 Oct 30;107(1):1–10. doi: 10.1016/0378-1119(91)90290-r. [DOI] [PubMed] [Google Scholar]
  9. Dagert M., Ehrlich S. D. Prolonged incubation in calcium chloride improves the competence of Escherichia coli cells. Gene. 1979 May;6(1):23–28. doi: 10.1016/0378-1119(79)90082-9. [DOI] [PubMed] [Google Scholar]
  10. DeVries C. A., Hassett D. J., Flynn J. L., Ohman D. E. Genetic linkage in Pseudomonas aeruginosa of algT and nadB: mutation in nadB does not affect NAD biosynthesis or alginate production. Gene. 1995 Apr 14;156(1):63–67. doi: 10.1016/0378-1119(95)00028-5. [DOI] [PubMed] [Google Scholar]
  11. DeVries C. A., Ohman D. E. Mucoid-to-nonmucoid conversion in alginate-producing Pseudomonas aeruginosa often results from spontaneous mutations in algT, encoding a putative alternate sigma factor, and shows evidence for autoregulation. J Bacteriol. 1994 Nov;176(21):6677–6687. doi: 10.1128/jb.176.21.6677-6687.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. Deretic V., Gill J. F., Chakrabarty A. M. Gene algD coding for GDPmannose dehydrogenase is transcriptionally activated in mucoid Pseudomonas aeruginosa. J Bacteriol. 1987 Jan;169(1):351–358. doi: 10.1128/jb.169.1.351-358.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Deretic V., Govan J. R., Konyecsni W. M., Martin D. W. Mucoid Pseudomonas aeruginosa in cystic fibrosis: mutations in the muc loci affect transcription of the algR and algD genes in response to environmental stimuli. Mol Microbiol. 1990 Feb;4(2):189–196. doi: 10.1111/j.1365-2958.1990.tb00586.x. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. Diver J. M., Bryan L. E., Sokol P. A. Transformation of Pseudomonas aeruginosa by electroporation. Anal Biochem. 1990 Aug 15;189(1):75–79. doi: 10.1016/0003-2697(90)90046-c. [DOI] [PubMed] [Google Scholar]
  17. Erickson J. W., Gross C. A. Identification of the sigma E subunit of Escherichia coli RNA polymerase: a second alternate sigma factor involved in high-temperature gene expression. Genes Dev. 1989 Sep;3(9):1462–1471. doi: 10.1101/gad.3.9.1462. [DOI] [PubMed] [Google Scholar]
  18. Evans L. R., Linker A. Production and characterization of the slime polysaccharide of Pseudomonas aeruginosa. J Bacteriol. 1973 Nov;116(2):915–924. doi: 10.1128/jb.116.2.915-924.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Farinha M. A., Kropinski A. M. Construction of broad-host-range plasmid vectors for easy visible selection and analysis of promoters. J Bacteriol. 1990 Jun;172(6):3496–3499. doi: 10.1128/jb.172.6.3496-3499.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Figurski D. H., Helinski D. R. Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc Natl Acad Sci U S A. 1979 Apr;76(4):1648–1652. doi: 10.1073/pnas.76.4.1648. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Flynn J. L., Ohman D. E. Cloning of genes from mucoid Pseudomonas aeruginosa which control spontaneous conversion to the alginate production phenotype. J Bacteriol. 1988 Apr;170(4):1452–1460. doi: 10.1128/jb.170.4.1452-1460.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Flynn J. L., Ohman D. E. Use of a gene replacement cosmid vector for cloning alginate conversion genes from mucoid and nonmucoid Pseudomonas aeruginosa strains: algS controls expression of algT. J Bacteriol. 1988 Jul;170(7):3228–3236. doi: 10.1128/jb.170.7.3228-3236.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Franklin M. J., Chitnis C. E., Gacesa P., Sonesson A., White D. C., Ohman D. E. Pseudomonas aeruginosa AlgG is a polymer level alginate C5-mannuronan epimerase. J Bacteriol. 1994 Apr;176(7):1821–1830. doi: 10.1128/jb.176.7.1821-1830.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Franklin M. J., Ohman D. E. Identification of algF in the alginate biosynthetic gene cluster of Pseudomonas aeruginosa which is required for alginate acetylation. J Bacteriol. 1993 Aug;175(16):5057–5065. doi: 10.1128/jb.175.16.5057-5065.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Friedman A. M., Long S. R., Brown S. E., Buikema W. J., Ausubel F. M. Construction of a broad host range cosmid cloning vector and its use in the genetic analysis of Rhizobium mutants. Gene. 1982 Jun;18(3):289–296. doi: 10.1016/0378-1119(82)90167-6. [DOI] [PubMed] [Google Scholar]
  26. Goldberg J. B., Dahnke T. Pseudomonas aeruginosa AlgB, which modulates the expression of alginate, is a member of the NtrC subclass of prokaryotic regulators. Mol Microbiol. 1992 Jan;6(1):59–66. doi: 10.1111/j.1365-2958.1992.tb00837.x. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. Goldberg J. B., Ohman D. E. Cloning and expression in Pseudomonas aeruginosa of a gene involved in the production of alginate. J Bacteriol. 1984 Jun;158(3):1115–1121. doi: 10.1128/jb.158.3.1115-1121.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Gorham H. C., McGowan S. J., Robson P. R., Hodgson D. A. Light-induced carotenogenesis in Myxococcus xanthus: light-dependent membrane sequestration of ECF sigma factor CarQ by anti-sigma factor CarR. Mol Microbiol. 1996 Jan;19(1):171–186. doi: 10.1046/j.1365-2958.1996.360888.x. [DOI] [PubMed] [Google Scholar]
  30. Govan J. R., Harris G. S. Pseudomonas aeruginosa and cystic fibrosis: unusual bacterial adaptation and pathogenesis. Microbiol Sci. 1986 Oct;3(10):302–308. [PubMed] [Google Scholar]
  31. Gutierrez C., Devedjian J. C. A plasmid facilitating in vitro construction of phoA gene fusions in Escherichia coli. Nucleic Acids Res. 1989 May 25;17(10):3999–3999. doi: 10.1093/nar/17.10.3999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Hershberger C. D., Ye R. W., Parsek M. R., Xie Z. D., Chakrabarty A. M. The algT (algU) gene of Pseudomonas aeruginosa, a key regulator involved in alginate biosynthesis, encodes an alternative sigma factor (sigma E). Proc Natl Acad Sci U S A. 1995 Aug 15;92(17):7941–7945. doi: 10.1073/pnas.92.17.7941. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Hiratsu K., Amemura M., Nashimoto H., Shinagawa H., Makino K. The rpoE gene of Escherichia coli, which encodes sigma E, is essential for bacterial growth at high temperature. J Bacteriol. 1995 May;177(10):2918–2922. doi: 10.1128/jb.177.10.2918-2922.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Holloway B. W., Morgan A. F. Genome organization in Pseudomonas. Annu Rev Microbiol. 1986;40:79–105. doi: 10.1146/annurev.mi.40.100186.000455. [DOI] [PubMed] [Google Scholar]
  35. Kreil G. Transfer of proteins across membranes. Annu Rev Biochem. 1981;50:317–348. doi: 10.1146/annurev.bi.50.070181.001533. [DOI] [PubMed] [Google Scholar]
  36. Lam J., Chan R., Lam K., Costerton J. W. Production of mucoid microcolonies by Pseudomonas aeruginosa within infected lungs in cystic fibrosis. Infect Immun. 1980 May;28(2):546–556. doi: 10.1128/iai.28.2.546-556.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Lonetto M. A., Brown K. L., Rudd K. E., Buttner M. J. Analysis of the Streptomyces coelicolor sigE gene reveals the existence of a subfamily of eubacterial RNA polymerase sigma factors involved in the regulation of extracytoplasmic functions. Proc Natl Acad Sci U S A. 1994 Aug 2;91(16):7573–7577. doi: 10.1073/pnas.91.16.7573. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Manoil C., Beckwith J. TnphoA: a transposon probe for protein export signals. Proc Natl Acad Sci U S A. 1985 Dec;82(23):8129–8133. doi: 10.1073/pnas.82.23.8129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Manoil C., Mekalanos J. J., Beckwith J. Alkaline phosphatase fusions: sensors of subcellular location. J Bacteriol. 1990 Feb;172(2):515–518. doi: 10.1128/jb.172.2.515-518.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Marcus H., Baker N. R. Quantitation of adherence of mucoid and nonmucoid Pseudomonas aeruginosa to hamster tracheal epithelium. Infect Immun. 1985 Mar;47(3):723–729. doi: 10.1128/iai.47.3.723-729.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Martin D. W., Holloway B. W., Deretic V. Characterization of a locus determining the mucoid status of Pseudomonas aeruginosa: AlgU shows sequence similarities with a Bacillus sigma factor. J Bacteriol. 1993 Feb;175(4):1153–1164. doi: 10.1128/jb.175.4.1153-1164.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Martin D. W., Schurr M. J., Mudd M. H., Govan J. R., Holloway B. W., Deretic V. Mechanism of conversion to mucoidy in Pseudomonas aeruginosa infecting cystic fibrosis patients. Proc Natl Acad Sci U S A. 1993 Sep 15;90(18):8377–8381. doi: 10.1073/pnas.90.18.8377. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Martin D. W., Schurr M. J., Yu H., Deretic V. Analysis of promoters controlled by the putative sigma factor AlgU regulating conversion to mucoidy in Pseudomonas aeruginosa: relationship to sigma E and stress response. J Bacteriol. 1994 Nov;176(21):6688–6696. doi: 10.1128/jb.176.21.6688-6696.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Mathee K., Howe M. M. Bacteriophage Mu Mor protein requires sigma 70 to activate the Mu middle promoter. J Bacteriol. 1993 Sep;175(17):5314–5323. doi: 10.1128/jb.175.17.5314-5323.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Mathee K., Howe M. M. Identification of a positive regulator of the Mu middle operon. J Bacteriol. 1990 Dec;172(12):6641–6650. doi: 10.1128/jb.172.12.6641-6650.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. May T. B., Shinabarger D., Maharaj R., Kato J., Chu L., DeVault J. D., Roychoudhury S., Zielinski N. A., Berry A., Rothmel R. K. Alginate synthesis by Pseudomonas aeruginosa: a key pathogenic factor in chronic pulmonary infections of cystic fibrosis patients. Clin Microbiol Rev. 1991 Apr;4(2):191–206. doi: 10.1128/cmr.4.2.191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. McIver K., Kessler E., Ohman D. E. Substitution of active-site His-223 in Pseudomonas aeruginosa elastase and expression of the mutated lasB alleles in Escherichia coli show evidence for autoproteolytic processing of proelastase. J Bacteriol. 1991 Dec;173(24):7781–7789. doi: 10.1128/jb.173.24.7781-7789.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Monday S. R., Schiller N. L. Alginate synthesis in Pseudomonas aeruginosa: the role of AlgL (alginate lyase) and AlgX. J Bacteriol. 1996 Feb;178(3):625–632. doi: 10.1128/jb.178.3.625-632.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Ogle J. W., Janda J. M., Woods D. E., Vasil M. L. Characterization and use of a DNA probe as an epidemiological marker for Pseudomonas aeruginosa. J Infect Dis. 1987 Jan;155(1):119–126. doi: 10.1093/infdis/155.1.119. [DOI] [PubMed] [Google Scholar]
  50. Ohman D. E., Chakrabarty A. M. Genetic mapping of chromosomal determinants for the production of the exopolysaccharide alginate in a Pseudomonas aeruginosa cystic fibrosis isolate. Infect Immun. 1981 Jul;33(1):142–148. doi: 10.1128/iai.33.1.142-148.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Raina S., Missiakas D., Georgopoulos C. The rpoE gene encoding the sigma E (sigma 24) heat shock sigma factor of Escherichia coli. EMBO J. 1995 Mar 1;14(5):1043–1055. doi: 10.1002/j.1460-2075.1995.tb07085.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Ramphal R., Pier G. B. Role of Pseudomonas aeruginosa mucoid exopolysaccharide in adherence to tracheal cells. Infect Immun. 1985 Jan;47(1):1–4. doi: 10.1128/iai.47.1.1-4.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Rehm B. H., Boheim G., Tommassen J., Winkler U. K. Overexpression of algE in Escherichia coli: subcellular localization, purification, and ion channel properties. J Bacteriol. 1994 Sep;176(18):5639–5647. doi: 10.1128/jb.176.18.5639-5647.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Rouvière P. E., De Las Peñas A., Mecsas J., Lu C. Z., Rudd K. E., Gross C. A. rpoE, the gene encoding the second heat-shock sigma factor, sigma E, in Escherichia coli. EMBO J. 1995 Mar 1;14(5):1032–1042. doi: 10.1002/j.1460-2075.1995.tb07084.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Schiller N. L., Monday S. R., Boyd C. M., Keen N. T., Ohman D. E. Characterization of the Pseudomonas aeruginosa alginate lyase gene (algL): cloning, sequencing, and expression in Escherichia coli. J Bacteriol. 1993 Aug;175(15):4780–4789. doi: 10.1128/jb.175.15.4780-4789.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Schurr M. J., Martin D. W., Mudd M. H., Deretic V. Gene cluster controlling conversion to alginate-overproducing phenotype in Pseudomonas aeruginosa: functional analysis in a heterologous host and role in the instability of mucoidy. J Bacteriol. 1994 Jun;176(11):3375–3382. doi: 10.1128/jb.176.11.3375-3382.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Schurr M. J., Yu H., Boucher J. C., Hibler N. S., Deretic V. Multiple promoters and induction by heat shock of the gene encoding the alternative sigma factor AlgU (sigma E) which controls mucoidy in cystic fibrosis isolates of Pseudomonas aeruginosa. J Bacteriol. 1995 Oct;177(19):5670–5679. doi: 10.1128/jb.177.19.5670-5679.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Schurr M. J., Yu H., Martinez-Salazar J. M., Boucher J. C., Deretic V. Control of AlgU, a member of the sigma E-like family of stress sigma factors, by the negative regulators MucA and MucB and Pseudomonas aeruginosa conversion to mucoidy in cystic fibrosis. J Bacteriol. 1996 Aug;178(16):4997–5004. doi: 10.1128/jb.178.16.4997-5004.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Schurr M. J., Yu H., Martinez-Salazar J. M., Hibler N. S., Deretic V. Biochemical characterization and posttranslational modification of AlgU, a regulator of stress response in Pseudomonas aeruginosa. Biochem Biophys Res Commun. 1995 Nov 22;216(3):874–880. doi: 10.1006/bbrc.1995.2703. [DOI] [PubMed] [Google Scholar]
  60. Schwarzmann S., Boring J. R. Antiphagocytic Effect of Slime from a Mucoid Strain of Pseudomonas aeruginosa. Infect Immun. 1971 Jun;3(6):762–767. doi: 10.1128/iai.3.6.762-767.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Selvaraj G., Fong Y. C., Iyer V. N. A portable DNA sequence carrying the cohesive site (cos) of bacteriophage lambda and the mob (mobilization) region of the broad-host-range plasmid RK2: a module for the construction of new cosmids. Gene. 1984 Dec;32(1-2):235–241. doi: 10.1016/0378-1119(84)90051-9. [DOI] [PubMed] [Google Scholar]
  62. Shinabarger D., May T. B., Boyd A., Ghosh M., Chakrabarty A. M. Nucleotide sequence and expression of the Pseudomonas aeruginosa algF gene controlling acetylation of alginate. Mol Microbiol. 1993 Sep;9(5):1027–1035. doi: 10.1111/j.1365-2958.1993.tb01232.x. [DOI] [PubMed] [Google Scholar]
  63. Simpson J. A., Smith S. E., Dean R. T. Alginate inhibition of the uptake of Pseudomonas aeruginosa by macrophages. J Gen Microbiol. 1988 Jan;134(1):29–36. doi: 10.1099/00221287-134-1-29. [DOI] [PubMed] [Google Scholar]
  64. Wozniak D. J., Ohman D. E. Involvement of the alginate algT gene and integration host factor in the regulation of the Pseudomonas aeruginosa algB gene. J Bacteriol. 1993 Jul;175(13):4145–4153. doi: 10.1128/jb.175.13.4145-4153.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Wozniak D. J., Ohman D. E. Pseudomonas aeruginosa AlgB, a two-component response regulator of the NtrC family, is required for algD transcription. J Bacteriol. 1991 Feb;173(4):1406–1413. doi: 10.1128/jb.173.4.1406-1413.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Wozniak D. J., Ohman D. E. Transcriptional analysis of the Pseudomonas aeruginosa genes algR, algB, and algD reveals a hierarchy of alginate gene expression which is modulated by algT. J Bacteriol. 1994 Oct;176(19):6007–6014. doi: 10.1128/jb.176.19.6007-6014.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Xie Z. D., Hershberger C. D., Shankar S., Ye R. W., Chakrabarty A. M. Sigma factor-anti-sigma factor interaction in alginate synthesis: inhibition of AlgT by MucA. J Bacteriol. 1996 Aug;178(16):4990–4996. doi: 10.1128/jb.178.16.4990-4996.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Yura T., Nagai H., Mori H. Regulation of the heat-shock response in bacteria. Annu Rev Microbiol. 1993;47:321–350. doi: 10.1146/annurev.mi.47.100193.001541. [DOI] [PubMed] [Google Scholar]
  69. Zielinski N. A., Chakrabarty A. M., Berry A. Characterization and regulation of the Pseudomonas aeruginosa algC gene encoding phosphomannomutase. J Biol Chem. 1991 May 25;266(15):9754–9763. [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES