Abstract
The extraordinary conservation of inorganic polyphosphate (polyP) in all cells - bacteria, fungi, plants and animals - and the various uses to which it might be put are reminiscent of the many ways in which other highly conserved molecules, such as ATP, NAD, fatty acids and certain polypeptides, have been exploited in evolution. A serious difficulty in understanding the physiological role of polyP has been the inadequacy of quantitative methods. With polyP-specific enzymatic assays and facile enrichment of polyP from crude extracts (see Chap. 12), it was observed that the accumulation and disappearance of polyP in Escherichia coli (and other organisms) are dynamic; fluctuations of 100- to 1000-fold are observed in response to nutritional and environmental stresses. These fluctuations depend on a global network of metabolic pathways. Insight into the metabolic roles for polyP in E. coli has been derived from mutant cells lacking PPK, the enzyme responsible for the synthesis of polyP. These roles establish an essential place for polyP in the regulation of responses to nutritional deficiencies, environmental stresses and survival in the stationary phase.
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References
Aiking H, Stijnman A, van Garderen C, Van Heerikhuizena H, van’t Riet J (1984) Inorganic phosphate accumulation and cadmium detoxification in Klebsiella aerogenes NCTC 418 growing in continuous culture. Appl Environ Microbiol 47: 374–377
Akiyama M, Crooke E, Kornberg A (1993) An exopolyphosphatase of Escherichia coli. The enyzme and its ppx gene in a polyphosphate operon. J Biol Chem 268: 633–639
Archibald FS, Fridovich I (1982) Investigations of the state of the manganese in Lactobacillus plantarum. Arch Biochem Biophys 215: 589–596
Ault-Riché D, Fraley CD, Tzeng C-M, Kornberg A (1998) Novel assay reveals multiple pathways regulating stress-induced accumulations of inorganic polyphosphate in Escherichia coli. J Bacteriol 180: 1841–1847
Cashel M, Gentry DR, Hernandez VJ, Vinella D (1996) The stringent response. In: Neidhardt FC, Curtiss R III, Ingraham JL, Lin ECC, Low KB, Magasanik B, Reznikoff WS, Riley M, Shaechter M, Umbarger HE (eds) Escherichia coli and Salmonella typhimurium: cellular and molecular biology. American Society for Microbiology, Washington, DC, pp 1458–1496
Chapman AG, Atkinson DE (1977) Adenine nucleotide concentrations and turnover rates. Their correlation with biological activity in bacteria and yeast. Adv Microb Physiol 15: 253–306
Crooke E, Akiyama M, Rao NN, Kornberg A (1994) Genetically altered levels of inorganic polyphosphate in Escherichia coli. J Biol Chem 269: 6290–6295
Demple B (1991) Regulation of bacterial oxidative stress genes. Annu Rev Genet 25: 315–337
Greenberg JT, Demple B (1988) Overproduction of peroxide-scavenging enzymes in Escherichia coli suppresses spontaneous mutagenesis and sensitivity to redox-cycling agents in oxy R mutants. EMBO J 7: 2611–2617
Hengge-Aronis R (1993) Survival of hunger and stress: the role of rpoS in early stationary phase gene regulation in E. coli Cell 72: 165–168
Irr JD (1972) Control of nucleotide metabolism and ribosomal ribonucleic acid synthesis during nitrogen starvation of Escherichia coli. J Bacteriol 110: 554–561
Jenkins DE, Chaisson SA, Matin A (1990) Starvation-induced cross protection against osmotic challenge in Escherichia coli. J Bacteriol 172: 2779–2781
Keasling JD, Hupf GA (1996) Genetic manipulation of polyphosphate metabolism affects cadmium tolerance in Escherichia coli. Appl Environ Microbiol 62: 743–746
Kolter R, Siegele DA, Tormo A (1993) The stationary phase of the bacterial life cycle. Annu Rev Microbiol 47: 855–874
Kuroda A, Murphy H, Cashel M, Kornberg A (1997) Guanosine tetra-and pentaphosphate promote accumulation of inorganic polyphosphate in Escherichia coli. J Biol Chem 272: 21240–21243
Lazzarini RA, Cashel M, Gallant J (1971) On the regulation of guanosine tetraphosphate levels in stringent and relaxed strains. J Biol Chem 246: 4381–4385
Loewen PC, Hengge-Aronis R (1994) The role of the sigma factor os (KatF) in bacterial global regulation. Annu Rev Microbiol 48: 53–80
Loewen PC, Switala J, Triggs-Raine BL (1985) Catalases HPI and HPII in Escherichia coli are induced independently. Arch Biochem Biophys 243: 144–149
Rachlin JW, Jenson TE, Baxter M, Jani V (1982) Utilization of morphometric analysis in evaluating response of Plectonema boryanum (Cyanophyceae) to eight heavy metals. Arch Environ Contam Toxicol 11: 323–333
Rao NN, Kornberg A (1996) Inorganic polyphosphate supports resistance and survival of stationary-phase Escherichia coli. J Bacteriol 178: 1394–1400
Rao NN, Liu S, Kornberg A (1998) Inorganic polyphosphate in Escherichia coli : the phosphate regulon and the stringent response. J Bacteriol 180: 2186–2193
Scott JA, Palmer SJ (1990) Sites of cadmium uptake in bacteria used for biosorption. Appl Microbiol Biotechnol 33: 221–225
Shiba T, Tsutsumi K, Yano H, Ihara Y, Kameda A, Tanaka K, Takahashi H, Munekata M, Rao NN, Kornberg A (1997) Inorganic polyphosphate and the induction of rpoS expression. Proc Natl Acad Sci USA 94: 11210–11215
Shinagawa H, Makino K, Amemura M, Nakata A (1987) Structure and function of the regulatory genes for the phosphate regulon in Escherichia coli. In: Torriani-Gorini A, Rothman FG, Silver S, Wright A, Yagil E (eds) Phosphate metabolism and cellular regulation in microorganisms. American Society for Microbiology, Washington, DC, pp 20–25
Sicko-Goad L, Lazinskiy D (1986) Quantitative ultrastructural changes associated with lead-coupled luxury phosphate uptake and polyphosphate utilization. Arch Environ Contam Toxicol 15: 617–627
Spira B, Silberstein N, Yagil E (1995) Guanosine 3’, 5’-bispyrophosphate (ppGpp) synthesis in cells of Escherichia coli starved for P. J Bacteriol 177: 4053–4058
Svitil AL, Cashel M, Zyskind JW (1993) Guanosine tetraphosphate inhibits protein synthesis in vivo. J Biol Chem 268: 2307–2311
Thor H, Smith MT, Hartzell P, Bellomo G, Jewell SA, Orrenius S (1982) The metabolism of menadione (2-methyl-1,4-naphthoquinone) by isolated hepatocytes. J Biol Chem 257: 12419–12425
Torriani-Gorini A (1994) Introduction: the Pho regulon of Escherichia coli. In: Torriani-Gorini A, Silver S, Yagil E (eds) Phosphate in microorganisms: cellular and molecular biology. American Society for Microbiology, Washington, DC, pp 1–4
Van Veen HW, Abee T, Kleefman AWF, Melgers B, Kortsee GJJ, Konings WN, Zehnder AJB (1994a) Energetics of alanine, lysine, and proline transport in cytoplasmic membranes of the polyphosphate-accumulating Acinetobacter johnsonii strain 210A. J Bacteriol 176: 2670–2676
Van Veen HW, Abee T, Periera H, Kortsee GJJ, Konings WN, Zehnder AJB (1994b) Generation of a proton motive force by the excretion of metal-phosphate in the polyphosphate-accumulating Acinetobacter johnsonii strain 210A. J Biol Chem 269: 29509–29514
Wanner BL (1994) Multiple controls of the Escherichia coli Pho regulon by the P, sensor PhoR, the catabolite regulatory sensor CreC, and acetyl phosphate. In: Torriani-Gorini A, Silver S, Yagil E (eds) Phosphate in microorganisms. cellular and molecular biology. American Society for Microbiology, Washington, DC, pp 13–21
Wanner BL (1995) Signal transduction and cross regulation in the Escherichia coli phosphate regulon by PhoR, CreC, and acetyl phosphate. In: Hoch JA, Silhavy TJ (eds) Two-component signal transduction. ASM Press, Washington, DC, pp 203–221
Wanner BL (1996) Phosphorus assimilation and control of the phosphate regulon. In: Neidhardt FC, Curtiss R III, Ingraham JL, Lin ECC, Low KB, Magasanik B, Reznikoff WS, Riley M, Shaechter M, Umbarger HE (eds) Escherichia coli and Salmonella typhimurium : cellular and molecular biology. American Society for Microbiology, Washington, DC, pp 1357–1381
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Rao, N.N., Kornberg, A. (1999). Inorganic Polyphosphate Regulates Responses of Escherichia coli to Nutritional Stringencies, Environmental Stresses and Survival in the Stationary Phase. In: Schröder, H.C., Müller, W.E.G. (eds) Inorganic Polyphosphates. Progress in Molecular and Subcellular Biology, vol 23. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-58444-2_9
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DOI: https://doi.org/10.1007/978-3-642-58444-2_9
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