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PMID: 7928963 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Energy metabolism and alginate biosynthesis in Pseudomonas aeruginosa: role of the tricarboxylic acid cycle.

Journal of bacteriology ·Vol. 176 ·No. 19 ·1994-10-00 ·Pages 6023-9

Schlictman D, Kavanaugh-Black A, Shankar S, Chakrabarty AM

Abstract

Infection with mucoid, alginate-producing strains of Pseudomonas aeruginosa is the leading cause of mortality among patients with cystic fibrosis. Alginate production by P. aeruginosa is not constitutive but is triggered by stresses such as starvation. The algR2 (also termed algQ) gene has been previously identified as being necessary for mucoidy; an algR2 mutant strain is unable to produce alginate when grown at 37 degrees C. We show here that the levels of phosphorylated succinyl coenzyme A synthetase (Scs) and nucleoside diphosphate kinase (Ndk), which form a complex in P. aeruginosa, are reduced in the algR2 mutant. We were able to correlate the lower level of phosphorylated Scs with a decrease in Scs activity. Western blots (immunoblots) also showed a decreased level of Ndk in the algR2 mutant, but the presence of another kinase activity sensitive to Tween 20 provides the missing Ndk function. The effect of AlgR2 on tricarboxylic acid (TCA) cycle enzymes appears to be specific for Scs, since none of the other TCA cycle enzymes measured showed a significant decrease in activity. Furthermore, the ability of the algR2 mutant to grow on TCA cycle intermediates, but not glucose, is impaired. These data indicate that AlgR2 is responsible for maintaining proper operation of the TCA cycle and energy metabolism.

Related Genes
MeSH Terms
Alginates/metabolism Bacterial Proteins/genetics Citric Acid Cycle Energy Metabolism Mutagenesis, Insertional Nucleoside-Diphosphate Kinase/metabolism Phosphorylation Protein Kinases/genetics Protein Processing, Post-Translational Pseudomonas aeruginosa/genetics,growth & development,metabolism Succinate-CoA Ligases/metabolism Trans-Activators
Chemicals
AlgQ protein, Pseudomonas aeruginosa Alginates Bacterial Proteins Trans-Activators Protein Kinases Nucleoside-Diphosphate Kinase Succinate-CoA Ligases
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Schlictman D
Department of Microbiology and Immunology, University of Illinois College of Medicine, Chicago 60612.
Kavanaugh-Black A
Shankar S
Chakrabarty A M
References (46)
46 references, click to expand
  1. Pyruvate kinase of Escherichia coli. Its role in supplying nucleoside triphosphates in cells under anaerobic conditions.
    J Biochem. 1974 Sep;76(3):631-7 PMID: 4373448
  2. Nucleoside diphosphate kinase from Myxococcus xanthus. I. Cloning and sequencing of the gene.
    J Biol Chem. 1990 Feb 15;265(5):2702-6 PMID: 2154455
  3. Regulation of the tricarboxylic acid cycle and poly-beta-hydroxybutyrate metabolism in Azotobacter beijerinckii grown under nitrogen or oxygen limitation.
    J Gen Microbiol. 1976 Dec;97(2):303-12 PMID: 13143
  4. Biosynthesis of exopolysaccharide by Pseudomonas aeruginosa.
    J Bacteriol. 1978 May;134(2):418-22 PMID: 96088
  5. 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):238-47 PMID: 6444976
  6. Production of mucoid microcolonies by Pseudomonas aeruginosa within infected lungs in cystic fibrosis.
    Infect Immun. 1980 May;28(2):546-56 PMID: 6772562
  7. Induction of citric acid cycle enzymes during initiation of sporulation by guanine nucleotide deprivation.
    J Bacteriol. 1981 Apr;146(1):337-44 PMID: 6783618
  8. Alginate synthesis in mucoid Pseudomonas aeruginosa: a chromosomal locus involved in control.
    J Gen Microbiol. 1980 Aug;119(2):443-50 PMID: 6785378
  9. 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):142-8 PMID: 6790439
  10. Influence of culture conditions on expression of the mucoid mode of growth of Pseudomonas aeruginosa.
    J Clin Microbiol. 1984 Jan;19(1):8-16 PMID: 6418765
  11. Cloning of genes controlling alginate biosynthesis from a mucoid cystic fibrosis isolate of Pseudomonas aeruginosa.
    J Bacteriol. 1984 Jul;159(1):9-18 PMID: 6330052
  12. Alternative pathways of carbohydrate utilization in pseudomonads.
    Annu Rev Microbiol. 1984;38:359-88 PMID: 6388497
  13. Molecular cloning of the plasmid RP4 primase region in a multi-host-range tacP expression vector.
    Gene. 1986;48(1):119-31 PMID: 3549457
  14. Relationship between aconitase gene expression and sporulation in Bacillus subtilis.
    J Bacteriol. 1987 Jul;169(7):3068-75 PMID: 3110134
  15. Identification of the promoter of the Bacillus subtilis sdh operon.
    J Bacteriol. 1987 Jul;169(7):3232-6 PMID: 3036777
  16. Cloning of genes from mucoid Pseudomonas aeruginosa which control spontaneous conversion to the alginate production phenotype.
    J Bacteriol. 1988 Apr;170(4):1452-60 PMID: 2965141
  17. Cloning and sequencing of two tandem genes involved in degradation of 2,3-dihydroxybiphenyl to benzoic acid in the polychlorinated biphenyl-degrading soil bacterium Pseudomonas sp. strain KKS102.
    J Bacteriol. 1989 May;171(5):2740-7 PMID: 2540155
  18. Control of mucoidy in Pseudomonas aeruginosa: transcriptional regulation of algR and identification of the second regulatory gene, algQ.
    J Bacteriol. 1989 Jul;171(7):3680-8 PMID: 2544550
  19. Nucleotide sequence of a regulatory region controlling alginate synthesis in Pseudomonas aeruginosa: characterization of the algR2 gene.
    Gene. 1989 Dec 7;84(1):31-8 PMID: 2514124
  20. Conversion of Pseudomonas aeruginosa to the phenotype characteristic of strains from patients with cystic fibrosis.
    J Clin Microbiol. 1990 Feb;28(2):188-94 PMID: 2107198
  21. Pulmonary dehydration and infection in cystic fibrosis: evidence that ethanol activates alginate gene expression and induction of mucoidy in Pseudomonas aeruginosa.
    Mol Microbiol. 1990 May;4(5):737-45 PMID: 2167423
  22. In vivo regulation of virulence in Pseudomonas aeruginosa associated with genetic rearrangement.
    J Infect Dis. 1991 Jan;163(1):143-9 PMID: 1824596
  23. Functional consequences of substitution of the active site (phospho)histidine residue of Escherichia coli succinyl-CoA synthetase.
    Biochim Biophys Acta. 1991 Jan 8;1076(1):86-90 PMID: 1986797
  24. Environmental conditions which influence mucoid conversion Pseudomonas aeruginosa PAO1.
    Infect Immun. 1991 Feb;59(2):471-7 PMID: 1898904
  25. Nucleoside diphosphate kinase from human erythrocytes. Structural characterization of the two polypeptide chains responsible for heterogeneity of the hexameric enzyme.
    J Biol Chem. 1991 May 15;266(14):8784-9 PMID: 1851158
  26. 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 PMID: 1906371
  27. Role of energy metabolism in conversion of nonmucoid Pseudomonas aeruginosa to the mucoid phenotype.
    Infect Immun. 1992 Apr;60(4):1329-35 PMID: 1372292
  28. Signal transduction in exopolysaccharide alginate synthesis: phosphorylation of the response regulator AlgR1 in Pseudomonas aeruginosa and Escherichia coli.
    Gene. 1992 Mar 1;112(1):45-51 PMID: 1551597
  29. Cystic fibrosis: molecular biology and therapeutic implications.
    Science. 1992 May 8;256(5058):774-9 PMID: 1375392
  30. Nucleoside diphosphokinase: a functional link between intermediary metabolism and nucleic acid synthesis.
    Curr Top Cell Regul. 1992;33:343-57 PMID: 1323446
  31. Alginate synthesis in Pseudomonas aeruginosa: environmental regulation of the algC promoter.
    J Bacteriol. 1992 Dec;174(23):7680-8 PMID: 1447138
  32. 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):1153-64 PMID: 8432708
  33. Autophosphorylation of nucleoside diphosphate kinase from Myxococcus xanthus.
    J Bacteriol. 1993 Feb;175(4):1176-81 PMID: 8381783
  34. Effect of different nutritional conditions on the synthesis of tricarboxylic acid cycle enzymes.
    J Bacteriol. 1967 Jun;93(6):1777-87 PMID: 4960893
  35. Enzymatic control of the metabolic activity of Pseudomonas aeruginosa grown in glucose or succinate media.
    Biochim Biophys Acta. 1969 Dec 30;192(3):395-401 PMID: 4312775
  36. Utilization of dicarboxylic acids by Pseudomonas aeruginosa.
    Can J Microbiol. 1969 Sep;15(9):1095-100 PMID: 4391940
  37. Culture medium for enterobacteria.
    J Bacteriol. 1974 Sep;119(3):736-47 PMID: 4604283
  38. Isolation and properties of a mutant of Escherichia coli with an insertional inactivation of the uspA gene, which encodes a universal stress protein.
    J Bacteriol. 1993 Jul;175(13):3949-56 PMID: 8391533
  39. Chromosomal mapping, expression and synthesis of lipopolysaccharide in Pseudomonas aeruginosa: a role for guanosine diphospho (GDP)-D-mannose.
    Mol Microbiol. 1993 May;8(4):771-82 PMID: 7687320
  40. Enhancer-like activity of A1gR1-binding site in alginate gene activation: positional, orientational, and sequence specificity.
    J Bacteriol. 1993 Sep;175(17):5452-9 PMID: 8366031
  41. Conversion to mucoidy in Pseudomonas aeruginosa.
    Biotechnology (N Y). 1993 Oct;11(10):1133-6 PMID: 7764093
  42. Genetic rearrangement associated with in vivo mucoid conversion of Pseudomonas aeruginosa PAO is due to insertion elements.
    J Bacteriol. 1994 Feb;176(3):553-62 PMID: 8300510
  43. Characterization of nucleoside-diphosphate kinase from Pseudomonas aeruginosa: complex formation with succinyl-CoA synthetase.
    Proc Natl Acad Sci U S A. 1994 Jun 21;91(13):5883-7 PMID: 8016083
  44. Pseudomonas aeruginosa: genes and enzymes of alginate synthesis.
    Trends Microbiol. 1994 May;2(5):151-7 PMID: 8055178
  45. Spectrophotometric measurements of the enzymatic formation of fumaric and cis-aconitic acids.
    Biochim Biophys Acta. 1950 Jan;4(1-3):211-4 PMID: 15403927
  46. Regulation of the dicarboxylic acid part of the citric acid cycle in Bacillus subtilis.
    J Bacteriol. 1975 Apr;122(1):224-34 PMID: 804468
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
1994-10-00
Pages
6023-9
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC196820
Subset
IM
Grants
NIAID NIH HHS · AI 16790-14 · United States
NIAID NIH HHS · AI 31546-02 · United States
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