Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1977 Oct;132(1):36–43. doi: 10.1128/jb.132.1.36-43.1977

Variations in the Adenylate Energy Charge During Phased Growth (Cell Cycle) of Candida utilis Under Energy Excess and Energy-Limiting Growth Conditions

K Chandapillai Thomas 1, Peter S S Dawson 1
PMCID: PMC221823  PMID: 562339

Abstract

The variations in the levels of adenine nucleotides during the phased growth (cell cycle) of the yeast Candida utilis growing under nitrogen, sulfate, or iron limitation with glycerol as carbon source have been determined. Synchronous cultures were obtained by the continuous phasing technique, and the results were compared with those of chemostat cultures growing at similar growth rates and under the same types of nutrient limitation. Whereas the chemostat experiments indicated only the average energy status of cultures growing at random, results from phased cultures showed that the adenylate energy charge, defined as (ATP + ½ADP)/(ATP + ADP + AMP) (where ATP, ADP, and AMP signify adenosine 5′-triphosphate, -diphosphate, and -monophosphate, respectively), varied during the phased growth of the yeast. These variations were related to the stage of development of the cells and to the type of nutrient limitation. In every case the energy charge dropped to a low value during the first half of the phasing cycle (cell cycle). Whereas the energy charge was maintained at relatively high levels (ranging from 0.78 to 0.94), for sulfate- or nitrogen-limited cultures, it was very low when iron was the growth-limiting nutrient (0.44 to 0.78). In spite of the low energy charge, the yeast continued to grow under iron limitation. The main component of the adenylate pool of the iron-limited culture was ADP and not ATP as observed with other types of nutrient limitation. It is concluded that under iron limitation the growth of the organism is limited by energy and that under energy-limited growth the energy charge of a growing organism is maintained at low levels. The reason for maintaining a low energy charge in an energy-limited culture is discussed.

Full text

PDF
36

Selected References

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

  1. Anagnostopoulos G. D. Unbalanced growth in a semi-continuous culture system designed for the synchronization of cell division. J Gen Microbiol. 1971 Jan;65(1):23–33. doi: 10.1099/00221287-65-1-23. [DOI] [PubMed] [Google Scholar]
  2. Atkinson D. E. Biochemical function and homeostasis: the payoff of the genetic program. Adv Exp Med Biol. 1975;62:193–211. doi: 10.1007/978-1-4684-3255-8_11. [DOI] [PubMed] [Google Scholar]
  3. Atkinson D. E. Regulation of enzyme function. Annu Rev Microbiol. 1969;23:47–68. doi: 10.1146/annurev.mi.23.100169.000403. [DOI] [PubMed] [Google Scholar]
  4. Bomsel J. L., Pradet A. Study of adenosine 5'-mono-,di- and triphosphates in plant tissues. IV. Regulation of the level of nucleotides, in vivo, by adenylate kinase: theoretical and experimental study. Biochim Biophys Acta. 1968 Aug 20;162(2):230–242. doi: 10.1016/0005-2728(68)90105-9. [DOI] [PubMed] [Google Scholar]
  5. Chapman A. G., Atkinson D. E. Stabilization of adenylate energy charge by the adenylate deaminase reaction. J Biol Chem. 1973 Dec 10;248(23):8309–8312. [PubMed] [Google Scholar]
  6. 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]
  7. Clegg R. A., Light P. A. Growth yields of Torulopsis utilis grown in continuous culture with glycerol or iron as the growth-limiting nutrient. Biochem J. 1971 Aug;124(1):152–154. doi: 10.1042/bj1240152. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dawson P. S. Continuous phased growth, with a modified chemostat. Can J Microbiol. 1965 Dec;11(6):893–903. doi: 10.1139/m65-119. [DOI] [PubMed] [Google Scholar]
  9. Dolezal J., Kaprálek F. Physiological characteristics of chemostatically grown Citrobacter freundii as a function of the specific growth rate and type of nutrient limitation. Folia Microbiol (Praha) 1976;21(3):168–177. doi: 10.1007/BF02883152. [DOI] [PubMed] [Google Scholar]
  10. Haddock B. A., Garland P. B. Effect of sulphate-limited growth on mitochondrial electron transfer and energy conservation between reduced nicotinamide-adenine dinucleotide and the cytochromes in Torulopsis utilis. Biochem J. 1971 Aug;124(1):155–170. doi: 10.1042/bj1240155. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Harrison D. E., Maitra P. K. Control of respiration and metabolism in growing Klebsiella aerogenes. The role of adenine nucleotides. Biochem J. 1969 May;112(5):647–656. doi: 10.1042/bj1120647. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Light P. A., Garland P. B. A comparison of mitochondria from Torulopsis utilis grown in continuous culture with glycerol, iron, ammonium, magnesium or phosphate as the growth-limiting nutrient. Biochem J. 1971 Aug;124(1):123–134. doi: 10.1042/bj1240123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. 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]
  14. Müller J., Dawson P. S. The operational flexibility of the phased culture technique, as observed by changes in the cell cycle of Candida utilis. Can J Microbiol. 1968 Oct;14(10):1115–1126. doi: 10.1139/m68-187. [DOI] [PubMed] [Google Scholar]
  15. Neijssel O. M., Tempest D. W. The role of energy-spilling reactions in the growth of Klebsiella aerogenes NCTC 418 in aerobic chemostat culture. Arch Microbiol. 1976 Nov 2;110(23):305–311. doi: 10.1007/BF00690243. [DOI] [PubMed] [Google Scholar]
  16. Polakis E. S., Bartley W. Changes in the intracellular concentrations of adenosine phosphates and nicotinamide nucleotides during the aerobic growth cycle of yeast on different carbon sources. Biochem J. 1966 Jun;99(3):521–533. doi: 10.1042/bj0990521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Santarius K. A., Heber U. Changes in the intracellular levels of ATP, ADP, AMP and P1 and regulatory function of the adenylate system in leaf cells during photosynthesis. Biochim Biophys Acta. 1965 May 25;102(1):39–54. doi: 10.1016/0926-6585(65)90201-3. [DOI] [PubMed] [Google Scholar]
  18. Schramm V. L., Leung H. Regulation of adenosine monophosphate levels as a function of adenosine triphosphate and inorganic phosphate. A proposed metabolic role for adenosine monophosphate nucleosidase from Azotobacter vinelandii. J Biol Chem. 1973 Dec 10;248(23):8313–8315. [PubMed] [Google Scholar]
  19. 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]

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

RESOURCES