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. 1979 Sep;139(3):792–799. doi: 10.1128/jb.139.3.792-799.1979

Consequences of Ca2+ deficiency on macromolecular synthesis and adenylate energy charge in Yersinia pestis.

R J Zahorchak, W T Charnetzky, R V Little, R R Brubaker
PMCID: PMC218024  PMID: 479109

Abstract

A 37 but not 26 degrees C virulent Yersinia pestis is known to require at least 2.5 mM Ca2+ for growth; this requirement is potentiated by Mg2+. After shift of log-phase cells (doubling time of 2 h) from 26 to 37 degrees C in Ca2+-deficient medium, shutoff of net ribonucleic acid synthesis preceded that of protein and cell mass. With 2.5 mM Mg2+, about two doublings in cell mass and number occurred before restriction with synthesis of sufficient deoxyribonucleic acid to account for initiation and termination of two postshift rounds of chromosome replication. Temperature shift with 20 mMMg2+ resulted in a single doubling of cell mass and number with one round of chromosome replication. Subsequent to shutoff of ribonucleic acid accumulation, ribonucleoside but not deoxyribonucleoside triphosphate pools became reduced to about 50% of normal values and the adenylate energy change fell from about 0.8, typical of growing cells, to about 0.6. Excretion of significant concentrations of adenine nucleotides under both permissive and restrictive conditions was observed. Only trace levels (less than 0.01 microM ol/g [dry weight]) of guaninosine 5'-diphosphate 3'-diphosphate accumulated under restrictive or permissive conditions; guanosine 5'-triphosphate 3'-diphosphate was not detected. Return of fully restricted cells from 37 to 26 degrees C with Ca2+ resulted in prompt growth, whereas addition of Ca2+ at 37 degrees C was ineffective. This finding indicates that the observed temperature-sensitive lesion in ribonucleic acid synthesis that results in restriction can be prevented but not reversed by cultivation with Ca2+.

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Selected References

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

  1. Adler L. W., Rosen B. P. Properties of Escherichia coli mutants with alterations in Mg2+-adenosine triphosphatase. J Bacteriol. 1976 Oct;128(1):248–256. doi: 10.1128/jb.128.1.248-256.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bagnara A. S., Finch L. R. Quantitative extraction and estimation of intracellular nucleoside triphosphates of Escherichia coli. Anal Biochem. 1972 Jan;45(1):24–34. doi: 10.1016/0003-2697(72)90004-8. [DOI] [PubMed] [Google Scholar]
  3. Beveridge T. J., Murray R. G. Uptake and retention of metals by cell walls of Bacillus subtilis. J Bacteriol. 1976 Sep;127(3):1502–1518. doi: 10.1128/jb.127.3.1502-1518.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Borle A. B. Calcium metabolism at the cellular level. Fed Proc. 1973 Sep;32(9):1944–1950. [PubMed] [Google Scholar]
  5. Brubaker R. R. Interconversion of Purine Mononucleotides in Pasteurella pestis. Infect Immun. 1970 May;1(5):446–454. doi: 10.1128/iai.1.5.446-454.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brubaker R. R. The genus Yersinia: biochemistry and genetics of virulence. Curr Top Microbiol Immunol. 1972;57:111–158. doi: 10.1007/978-3-642-65297-4_4. [DOI] [PubMed] [Google Scholar]
  7. Buckmire F. L., Murray R. G. Substructure and in vitro assembly of the outer, structured layer of Spirillum serpens. J Bacteriol. 1976 Jan;125(1):290–299. doi: 10.1128/jb.125.1.290-299.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cashel M. The control of ribonucleic acid synthesis in Escherichia coli. IV. Relevance of unusual phosphorylated compounds from amino acid-starved stringent strains. J Biol Chem. 1969 Jun 25;244(12):3133–3141. [PubMed] [Google Scholar]
  9. Chapman A. G., Fall L., Atkinson D. E. Adenylate energy charge in Escherichia coli during growth and starvation. J Bacteriol. 1971 Dec;108(3):1072–1086. doi: 10.1128/jb.108.3.1072-1086.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Cosloy S. D., Oishi M. Genetic transformation in Escherichia coli K12. Proc Natl Acad Sci U S A. 1973 Jan;70(1):84–87. doi: 10.1073/pnas.70.1.84. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dias F. F., Okrend H., Dondero N. C. Calcium nutrition of Sphaerotilus growing in a continuous-flow apparatus. Appl Microbiol. 1968 Sep;16(9):1364–1369. doi: 10.1128/am.16.9.1364-1369.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. HIGUCHI K., KUPFERBERG L. L., SMITH J. L. Studies on the nutrition and physiology of Pasteurella pestis. III. Effects of calcium ions on the growth of virulent and avirulent strains of Pasteurella pestis. J Bacteriol. 1959 Mar;77(3):317–321. doi: 10.1128/jb.77.3.317-321.1959. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. HIGUCHI K., SMITH J. L. Studies on the nutrition and physiology of Pasteurella pestis. VI. A differential plating medium for the estimation of the mutation rate to avirulence. J Bacteriol. 1961 Apr;81:605–608. doi: 10.1128/jb.81.4.605-608.1961. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hall P. J., Yang G. C., Little R. V., Brubaker R. R. Effect of Ca2+ on morphology and division of Yersinia pestis. Infect Immun. 1974 Jun;9(6):1105–1113. doi: 10.1128/iai.9.6.1105-1113.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kahane I., Ne'eman Z., Razin S. Divalent cations in native and reaggregated mycoplasma membranes. J Bacteriol. 1973 Feb;113(2):666–671. doi: 10.1128/jb.113.2.666-671.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kojima M., Suda S., Hotta S., Hamada K. Induction of pleomorphy and calcium ion deficiency in Lactobacillus bifidus. J Bacteriol. 1970 Apr;102(1):217–220. doi: 10.1128/jb.102.1.217-220.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kung F. C., Raymond J., Glaser D. A. Metal ion content of Escherichia coli versus cell age. J Bacteriol. 1976 Jun;126(3):1089–1095. doi: 10.1128/jb.126.3.1089-1095.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. LAWTON W. D., ERDMAN R. L., SURGALLA M. J. BIOSYNTHESIS AND PURIFICATION OF V AND W ANTIGEN IN PASTEURELLA PESTIS. J Immunol. 1963 Aug;91:179–184. doi: 10.21236/ad0299868. [DOI] [PubMed] [Google Scholar]
  19. Lehninger A. L. Mitochondria and calcium ion transport. Biochem J. 1970 Sep;119(2):129–138. doi: 10.1042/bj1190129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lundin A., Thore A. Comparison of methods for extraction of bacterial adenine nucleotides determined by firefly assay. Appl Microbiol. 1975 Nov;30(5):713–721. doi: 10.1128/am.30.5.713-721.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Nielsen R., Rasmussen H. Fractionation of extracts of firefly tails by gel filtration. Acta Chem Scand. 1968;22(6):1757–1762. doi: 10.3891/acta.chem.scand.22-1757. [DOI] [PubMed] [Google Scholar]
  22. Nierlich D. P. Regulation of bacterial growth, RNA, and protein synthesis. Annu Rev Microbiol. 1978;32:393–432. doi: 10.1146/annurev.mi.32.100178.002141. [DOI] [PubMed] [Google Scholar]
  23. Page W. J., Sadoff H. L. Relationship between calcium and uroinic acids in the encystment of Azotobacter vinelandii. J Bacteriol. 1975 Apr;122(1):145–151. doi: 10.1128/jb.122.1.145-151.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Papahadjopoulos D., Portis A., Pangborn W. Calcium-induced lipid phase transitions and membrane fusion. Ann N Y Acad Sci. 1978;308:50–66. doi: 10.1111/j.1749-6632.1978.tb22013.x. [DOI] [PubMed] [Google Scholar]
  25. Park M. H., Wong B. B., Lusk J. E. Mutants in three genes affecting transport of magnesium in Escherichia coli: genetics and physiology. J Bacteriol. 1976 Jun;126(3):1096–1103. doi: 10.1128/jb.126.3.1096-1103.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. ROODYN D. B., MANDEL H. G. A simple membrane fractionation method for determining the distribution of radioactivity in chemical fractions of Bacillus cereus. Biochim Biophys Acta. 1960 Jun 17;41:80–88. doi: 10.1016/0006-3002(60)90371-1. [DOI] [PubMed] [Google Scholar]
  27. Schulz H. The importance of carboxyl groups for the biological activity of acyl carrier protein of Escherichia coli. Biochem Biophys Res Commun. 1972 Feb 16;46(3):1446–1453. doi: 10.1016/s0006-291x(72)80139-6. [DOI] [PubMed] [Google Scholar]
  28. Seto H., Tomasz A. Calcium-requiring step in the uptake of deoxyribonucleic acid molecules through the surface of competent pneumococci. J Bacteriol. 1976 Jun;126(3):1113–1118. doi: 10.1128/jb.126.3.1113-1118.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Silver S., Clark D. Magnesium transport in Escherichia coli. J Biol Chem. 1971 Feb 10;246(3):569–576. [PubMed] [Google Scholar]
  30. Silver S., Johnseine P., King K. Manganese Active Transport in Escherichia coli. J Bacteriol. 1970 Dec;104(3):1299–1306. doi: 10.1128/jb.104.3.1299-1306.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Silver S., Toth K., Scribner H. Facilitated transport of calcium by cells and subcellular membranes of Bacillus subtilis and Escherichia coli. J Bacteriol. 1975 Jun;122(3):880–885. doi: 10.1128/jb.122.3.880-885.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Sjöström J. E., Lindberg M., Philipson L. Transfection of Staphylococcus aureus with bacteriophage deoxyribonucleic acid. J Bacteriol. 1972 Jan;109(1):285–291. doi: 10.1128/jb.109.1.285-291.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Sloan J. B., Urban J. E. Growth response of Escherichia coli to nutritional shift-up: immediate division stimulation in slow-growing cells. J Bacteriol. 1976 Oct;128(1):302–308. doi: 10.1128/jb.128.1.302-308.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Snellen J. E., Raj H. D. Morphogenesis and fine structure of Leucothrix mucor and effects of calcium deficiency. J Bacteriol. 1970 Jan;101(1):240–249. doi: 10.1128/jb.101.1.240-249.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Stanley P. E., Williams S. G. Use of the liquid scintillation spectrometer for determining adenosine triphosphate by the luciferase enzyme. Anal Biochem. 1969 Jun;29(3):381–392. doi: 10.1016/0003-2697(69)90323-6. [DOI] [PubMed] [Google Scholar]
  36. Swedes J. S., Sedo R. J., Atkinson D. E. Relation of growth and protein synthesis to the adenylate energy charge in an adenine-requiring mutant of Escherichia coli. J Biol Chem. 1975 Sep 10;250(17):6930–6938. [PubMed] [Google Scholar]
  37. Yang G. C., Brubaker R. R. Effect of ca on the synthesis of deoxyribonucleic Acid in virulent and avirulent yersinia. Infect Immun. 1971 Jan;3(1):59–65. doi: 10.1128/iai.3.1.59-65.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]

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