Kinetic Analysis by in Vivo 31P Nuclear Magnetic Resonance of Internal Pi During the Uptake of Sn-glycerol-3-phosphate by the Pho Regulon-dependent Ugp System and the Glp Regulon-dependent GlpT System

Overview

Journal J Bacteriol

Publisher American Society for Microbiology

Specialty Microbiology

Date 1995 Feb 1

PMID 7836304

Citations 13

Authors

K B Xavier

M Kossmann

H Santos

W Boos

Affiliations

Soon will be listed here.

Abstract

When sn-glycerol-3-phosphate (G3P) is taken up exclusively by the pho regulon-dependent Ugp transport system, it can be used as the sole source of Pi but not as the sole source of carbon. We had previously suggested that the inability of G3P to be used as a carbon source under these conditions is due to trans inhibition of G3P uptake by internal Pi derived from the degradation of G3P (P. Brzoska, M. Rimmele, K. Brzostek, and W. Boos, J. Bacteriol. 176:15-20, 1994). Here we report 31P nuclear magnetic resonance measurements of intact cells after exposure to G3P as well as to Pi, using different mutants defective in pst (high-affinity Pi transport), ugp (pho-dependent G3P transport), glpT (glp-dependent G3P transport), and glpD (aerobic G3P dehydrogenase). When G3P was transported by the Ugp system and when metabolism of G3P was allowed (glpD+), Pi accumulated to about 13 to 19 mM. When G3P was taken up by the GlpT system, the preexisting internal Pi pool (whether low or high) did not change. Both systems were inversely controlled by internal Pi. Whereas the Ugp system was inhibited, the GlpT system was stimulated by elevated internal Pi.

Citing Articles

Context-dependent change in the fitness effect of (in)organic phosphate antiporter glpT during Salmonella Typhimurium infection.

Santamaria de Souza N, Cherrak Y, Andersen T, Vetsch M, Barthel M, Kroon S Nat Commun. 2025; 16(1):1912.

PMID: 39994176 PMC: 11850910. DOI: 10.1038/s41467-025-56851-5.

Thermodynamics shape the enzyme burden of glycolytic pathways.

Khana D, Jen A, Shishkova E, Thusoo E, Williams J, Henkel A bioRxiv. 2025; .

PMID: 39974948 PMC: 11838459. DOI: 10.1101/2025.01.31.635972.

An intracellular phosphorus-starvation signal activates the PhoB/PhoR two-component system in .

Bruna R, Kendra C, Pontes M mBio. 2024; 15(9):e0164224.

PMID: 39152718 PMC: 11389368. DOI: 10.1128/mbio.01642-24.

Phosphorus starvation response and PhoB-independent utilization of organic phosphate sources by .

Bruna R, Kendra C, Pontes M Microbiol Spectr. 2023; 11(6):e0226023.

PMID: 37787565 PMC: 10715179. DOI: 10.1128/spectrum.02260-23.

Comparison of Phenotype Nutritional Profiles and Phosphate Metabolism Genes in Four Serovars of from Water Sources.

Gorski L, Aviles Noriega A Microorganisms. 2023; 11(8).

PMID: 37630669 PMC: 10459026. DOI: 10.3390/microorganisms11082109.

References

Argast M, Boos W . Co-regulation in Escherichia coli of a novel transport system for sn-glycerol-3-phosphate and outer membrane protein Ic (e, E) with alkaline phosphatase and phosphate-binding protein. J Bacteriol. 1980; 143(1):142-50. PMC: 294198. DOI: 10.1128/jb.143.1.142-150.1980. View

Garen A, Levinthal C . A fine-structure genetic and chemical study of the enzyme alkaline phosphatase of E. coli. I. Purification and characterization of alkaline phosphatase. Biochim Biophys Acta. 1960; 38:470-83. DOI: 10.1016/0006-3002(60)91282-8. View

Schweizer H, Argast M, Boos W . Characteristics of a binding protein-dependent transport system for sn-glycerol-3-phosphate in Escherichia coli that is part of the pho regulon. J Bacteriol. 1982; 150(3):1154-63. PMC: 216336. DOI: 10.1128/jb.150.3.1154-1163.1982. View

Larson T, Schumacher G, Boos W . Identification of the glpT-encoded sn-glycerol-3-phosphate permease of Escherichia coli, an oligomeric integral membrane protein. J Bacteriol. 1982; 152(3):1008-21. PMC: 221604. DOI: 10.1128/jb.152.3.1008-1021.1982. View

Elvin C, Hardy C, Rosenberg H . Pi exchange mediated by the GlpT-dependent sn-glycerol-3-phosphate transport system in Escherichia coli. J Bacteriol. 1985; 161(3):1054-8. PMC: 215006. DOI: 10.1128/jb.161.3.1054-1058.1985. View

Ambudkar S, Larson T, Maloney P . Reconstitution of sugar phosphate transport systems of Escherichia coli. J Biol Chem. 1986; 261(20):9083-6. View

Elvin C, Dixon N, Rosenberg H . Molecular cloning of the phosphate (inorganic) transport (pit) gene of Escherichia coli K12. Identification of the pit+ gene product and physical mapping of the pit-gor region of the chromosome. Mol Gen Genet. 1986; 204(3):477-84. DOI: 10.1007/BF00331028. View

Larson T, Ye S, Weissenborn D, Hoffmann H, Schweizer H . Purification and characterization of the repressor for the sn-glycerol 3-phosphate regulon of Escherichia coli K12. J Biol Chem. 1987; 262(33):15869-74. View

Casadaban M . Transposition and fusion of the lac genes to selected promoters in Escherichia coli using bacteriophage lambda and Mu. J Mol Biol. 1976; 104(3):541-55. DOI: 10.1016/0022-2836(76)90119-4. View

10.

Ugurbil K, Rottenberg H, Glynn P, Shulman R . 31P nuclear magnetic resonance studies of bioenergetics and glycolysis in anaerobic Escherichia coli cells. Proc Natl Acad Sci U S A. 1978; 75(5):2244-8. PMC: 392528. DOI: 10.1073/pnas.75.5.2244. View

11.

Argast M, Ludtke D, Silhavy T, Boos W . A second transport system for sn-glycerol-3-phosphate in Escherichia coli. J Bacteriol. 1978; 136(3):1070-83. PMC: 218543. DOI: 10.1128/jb.136.3.1070-1083.1978. View

12.

Argast M, Boos W . Purification and properties of the sn-glycerol 3-phosphate-binding protein of Escherichia coli. J Biol Chem. 1979; 254(21):10931-5. View

13.

Overduin P, Boos W, Tommassen J . Nucleotide sequence of the ugp genes of Escherichia coli K-12: homology to the maltose system. Mol Microbiol. 1988; 2(6):767-75. DOI: 10.1111/j.1365-2958.1988.tb00088.x. View

14.

Lin E, Iuchi S . Regulation of gene expression in fermentative and respiratory systems in Escherichia coli and related bacteria. Annu Rev Genet. 1991; 25:361-87. DOI: 10.1146/annurev.ge.25.120191.002045. View

15.

Rao N, Roberts M, TORRIANI A, YASHPHE J . Effect of glpT and glpD mutations on expression of the phoA gene in Escherichia coli. J Bacteriol. 1993; 175(1):74-9. PMC: 196098. DOI: 10.1128/jb.175.1.74-79.1993. View

16.

Wanner B . Gene regulation by phosphate in enteric bacteria. J Cell Biochem. 1993; 51(1):47-54. DOI: 10.1002/jcb.240510110. View

17.

Hartmann A, Boos W . Mutations in phoB, the positive gene activator of the pho regulon in Escherichia coli, affect the carbohydrate phenotype on MacConkey indicator plates. Res Microbiol. 1993; 144(4):285-93. DOI: 10.1016/0923-2508(93)90013-r. View

18.

Brzoska P, Rimmele M, Brzostek K, Boos W . The pho regulon-dependent Ugp uptake system for glycerol-3-phosphate in Escherichia coli is trans inhibited by Pi. J Bacteriol. 1994; 176(1):15-20. PMC: 205009. DOI: 10.1128/jb.176.1.15-20.1994. View

19.

Kadner R, Webber C, Island M . The family of organo-phosphate transport proteins includes a transmembrane regulatory protein. J Bioenerg Biomembr. 1993; 25(6):637-45. DOI: 10.1007/BF00770251. View

20.

Hayashi S, Koch J, Lin E . ACTIVE TRANSPORT OF L-ALPHA-GLYCEROPHOSPHATE IN ESCHERICHIA COLI. J Biol Chem. 1964; 239:3098-105. View