Skip to main content
SpringerLink
Log in

Oscillations in Yeast Glycolysis

  • Chapter
  • First Online:
Physics of Biological Oscillators

Part of the book series: Understanding Complex Systems ((UCS))

Abstract

Oscillations in yeast glycolysis have been known for more than six decades. In spite of intensive experimental and model studies there are still gaps in our understanding of these glycolytic oscillations, e.g. the mechanisms by which they arise, why they have been preserved throughout evolution, and what their potential functions in the cell could be. In the current paper new experimental observations will be presented showing that many variables, that were hitherto considered unrelated to glycolysis, oscillate synchronously with glycolytic intermediates. Furthermore, a strong coupling between glycolysis and the polarisation of intracellular water  is presented, suggesting that water has a strong influence on metabolism. This challenges our current understanding of the mechanism behind the glycolytic oscillations. Finally, it is proposed that the function of metabolic oscillations is to maintain the cell in a state of constant low entropy.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 99.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 129.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 129.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. J. Aldridge, E. Pye, Cell density dependence of oscillatory metabolism. Nature 259(5545), 670–671 (1976)

    Article  ADS  Google Scholar 

  2. A.Z. Andersen, A.K. Poulsen, J.C. Brasen, L.F. Olsen, On-line measurements of oscillating mitochondrial membrane potential in glucose-fermenting Saccharomyces cerevisiae. Yeast 24(9), 731–739 (2007)

    Article  Google Scholar 

  3. M. Aon et al., Dynamic regulation of yeast glycolytic oscillations by mitochondrial functions. J. Cell Sci. 99(2), 325–334 (1991)

    Article  Google Scholar 

  4. M. Aon, S. Cortassa, H. Westerhoff, K. van Dam, Synchrony and mutual stimulation of yeast-cells during fast glycolytic oscillations. J. Gen. Microbiol. 138(10), 2219–2227 (1992)

    Article  Google Scholar 

  5. L.A. Bagatolli, Laurdan fluorescence properties in membranes: a journey from the fluorometer to the microscope, in Fluorescent Methods to Study Biological Membranes, ed. by Y. Mely, G. Duportail (Springer, Berlin, Heidelberg, 2013), pp. 3–35

    Google Scholar 

  6. L.A. Bagatolli, R.P. Stock, The use of 6-acyl-2-(dimethylamino)naphthalenes as relaxation probes of biological environments, in Perspectives on Fluorescence: A Tribute to Gregorio Weber, Springer Series in Fluorescence, ed. by D.M. Jameson (Springer, Heidelberg, 2016), pp. 197–216

    Google Scholar 

  7. S.F. Banani, H.O. Lee, A.A. Hyman, M.K. Rosen, Biomolecular condensates: organizers of cellular biochemistry. Nature Rev. Mol. Cell Biol. 18(5), 285–298 (2017)

    Article  Google Scholar 

  8. C. Bernard, Introduction a l’etude de la medicine experimentale (Macmillan, New York, 1927)

    Google Scholar 

  9. A. Betz, B. Chance, Influence of inhibitors and temperature on oscillation of reduced pyridine nucleotides in yeast cells. Arch. Biochem. Biophys. 109(3), 579–584 (1965)

    Article  Google Scholar 

  10. C.P. Brangwynne, T.J. Mitchison, A.A. Hyman, Active liquid-like behavior of nucleoli determines their size and shape in xenopus laevis oocytes. Proc. Natl. Acad. Sci. 108(11), 4334–4339 (2011)

    Article  ADS  Google Scholar 

  11. B. Chance, R. Estabrook, A. Ghosh, Damped sinusoidal oscillations of cytoplasmic reduced pyridine nucleotide in yeast cells. Proc. Natl. Acad. Sci. USA 51(6), 1244+ (1964)

    Google Scholar 

  12. B. Chance et al., Synchronization phenomena in oscillations of yeast cells and isolated mitochondria, in Biological and Biochemical Oscillators, ed. by B. Chance (Academic Press, New York, 1973), pp. 285–300

    Google Scholar 

  13. F.A. Chandra, G. Buzi, J.C. Doyle, Glycolytic oscillations and limits on robust efficiency. Science 333(6039), 187–192 (2011)

    Article  ADS  MathSciNet  MATH  Google Scholar 

  14. M. Chaplin, Do we underestimate the importance of water in cell biology? Nat. Rev. Mol. Cell Biol. 7(11), 861–866 (2006)

    Article  Google Scholar 

  15. N.A. Chebotareva, B.I. Kurganov, N.B. Livanova, Biochemical effects of molecular crowding. Biochemistry (Moscow) 69(11), 1239–1251 (2004)

    Article  Google Scholar 

  16. J. Clegg, Properties and metabolism of the aqueous cytoplasm and its boundaries. Am. J. Physiol. 246(2), R133–R151 (1984)

    Google Scholar 

  17. R.M. Davidson, A. Lauritzen, S. Seneff, Biological water dynamics and entropy: a biophysical origin of cancer and other diseases. Entropy 15(9), 3822–3876 (2013)

    Article  ADS  Google Scholar 

  18. H. Degn, Oscillating chemical reactions in homogeneous phase. J. Chem. Educ. 49(5), 302–307 (1972)

    Article  Google Scholar 

  19. B.J.T. Dodd, J.M. Kralj, Live cell imaging reveals pH oscillations in Saccharomyces cerevisiae during metabolic transitions. Sci. Rep. 7, 13992 (2017)

    Article  Google Scholar 

  20. L. Duysens, J. Amesz, Fluorescence spectrophotometry of reduced phosphopyridine nucleotide in intact cells in the near-ultraviolet and visible region. Biochim. Biophys. Acta 24, 19–26 (1957)

    Article  Google Scholar 

  21. R. Ellis, Macromolecular crowding: obvious but underappreciated. Trends Biochem. Sci. 26(10), 597–604 (2001)

    Article  Google Scholar 

  22. A. Ghosh, B. Chance, Oscillations of glycolytic intermediates in yeast cells. Biochem. Biophys. Res. Commun. 16(2), 174–181 (1964)

    Article  Google Scholar 

  23. A. Goldbeter, Biochemical Oscillations and Cellular Rhythms: The Molecular Bases of Periodic and Chaotic Behaviour (Cambridge University Press, Cambridge, 1996)

    Book  MATH  Google Scholar 

  24. A. Goldbeter, C. Gerard, D. Gonze, J.C. Leloup, G. Dupont, Systems biology of cellular rhythms. FEBS Lett. 586(18, SI), 2955–2965 (2012)

    Google Scholar 

  25. T. Heimburg, Linear nonequilibrium thermodynamics of reversible periodic processes and chemical oscillations. Phys. Chem. Chem. Phys. 19(26), 17331–17341 (2017)

    Article  Google Scholar 

  26. G. Karreman, Cooperative specific adsorption of ions at charged sites in an electric field. Bull. Math. Biophys. 27, 91–104 (1965)

    Article  Google Scholar 

  27. H. Knull, A.P. Minton, Structure within eukaryotic cytoplasm and its relationship to glycolytic metabolism. Cell Biochem. Funct. 14(4), 237–248 (1996)

    Article  Google Scholar 

  28. D. Kondepudi, I. Prigogine, Modern Thermodynamics: From Heat Engines to Dissipative Structures (Wiley, New York, 1998)

    MATH  Google Scholar 

  29. G. Ling, The association-induction hypothesis. Tex. Rep. Biol. Med. 22, 244–265 (1964)

    Google Scholar 

  30. G.N. Ling, The physical state of water in living cell and model systems. Ann. N. Y. Acad. Sci. 2, 401–417 (1965)

    ADS  Google Scholar 

  31. G. Ling, Diphosphoglycerate and inosine hexaphosphate control of oxygen binding by hemoglobin: a theoretical interpretation of experimental data. Proc. Natl. Acad. Sci. USA 67, 296–301 (1970)

    Article  ADS  Google Scholar 

  32. G.N. Ling, Life at the Cell and Below-cell Level: The Hidden History of a Fundamental Revolution in Biology (Pacific Press, New York, NY, 2001)

    Google Scholar 

  33. G. Ling, What is life answered in terms of properties and activities of autocooperative assemblies of molecules, atoms, ions, and electrons called nano-protoplasm. Physiol. Chem. Phys. Med. NMR 42, 1–64 (2012)

    ADS  Google Scholar 

  34. D. Lloyd, D. Murray, The temporal architecture of eukaryotic growth. FEBS Lett. 580(12, SI), 2830–2835 (2006)

    Google Scholar 

  35. D. Lloyd, M.A. Aon, S. Cortassa, Why homeodynamics, not homeostasis. Sci. World J. 1, 133–145 (2001)

    Article  Google Scholar 

  36. D. Lloyd, S. Cortassa, B. O’Rourke, M.A. Aon, What yeast and cardiomyocytes share: ultradian oscillatory redox mechanisms of cellular coherence and survival. Integr. Biol. 4(1), 65–74 (2012)

    Article  Google Scholar 

  37. C. Lu, D. Prada-Gracia, F. Rao, Structure and dynamics of water in crowded environments slows down peptide conformational changes. J. Chem. Phys. 141(4), 045101 (2014)

    Article  ADS  Google Scholar 

  38. K. Luby-Phelps, Cytoarchitecture and physical properties of cytoplasm: volume, viscosity. diffusion, intracellular surface area. Int. Rev. Cytol. 192, 189–221 (2000)

    Article  Google Scholar 

  39. R.B. Macgregor, G. Weber, Fluorophores in polar media: spectral effects of the Langevin distribution of electrostatic interactions. Ann. N. Y. Acad. Sci. 366, 140–154 (1981)

    Article  ADS  Google Scholar 

  40. P.K. Maitra, Pulsating glucose flux in yeast. Biochem. Biophys. Res. Commun. 25(4), 462–467 (1966)

    Article  Google Scholar 

  41. P.K. Maitra, R.W. Estabrook, Fluorometric method for enzymic determination of glycolytic intermediates. Anal. Biochem. 7(4), 472–484 (1964)

    Article  Google Scholar 

  42. T. Male, J. Feder, G.N. Giaever, I. Giaever, Oscillations in yeast observed electrically. Biol. Rhythm Res. 30(4), 361–370 (1999)

    Article  Google Scholar 

  43. A. Minta, R. Tsien, Fluorescent indicators for cytosolic sodium. J. Biol. Chem. 264(32), 19449–19457 (1989)

    Article  Google Scholar 

  44. G. Nicolis, J. Portnow, Chemical oscillations. Chem. Rev. 73(4), 365–384 (1973)

    Article  Google Scholar 

  45. G. Nicolis, I. Prigogine, Self-organization in Nonequilibrium Systems: From Dissipative Structures to Order Through Fluctuatons (Wiley, New York, 1977)

    MATH  Google Scholar 

  46. L.F. Olsen, A.Z. Andersen, A. Lunding, J.C. Brasen, A.K. Poulsen, Regulation of glycolytic oscillations by mitochondrial and plasma membrane H+-atpases. Biophys. J. 96(9), 3850–3861 (2009)

    Article  ADS  Google Scholar 

  47. L.F. Olsen, R.P. Stock, L. Bagatolli, Glycolytic oscillations and intracellular K+ concentration are strongly coupled in the yeast Saccharomyces cerevisiae. Arch. Biochem. Biophys. 681, 108257 (2020)

    Article  Google Scholar 

  48. L. Onsager, Reciprocal relations in irreversible processes. I. Phys. Rev. 37(4), 405–426 (1931)

    Article  ADS  MATH  Google Scholar 

  49. L. Onsager, Reciprocal relations in irreversible processes. II. Phys. Rev. 38(12), 2265–2279 (1931)

    Article  ADS  MATH  Google Scholar 

  50. V.C. Özalp, T.R. Pedersen, L.J. Nielsen, L.F. Olsen, Time-resolved measurements of intracellular ATP in the yeast Saccharomyces cerevisiae using a new type of nanobiosensor. J. Biol. Chem. 285(48), 37579–37588 (2010)

    Article  Google Scholar 

  51. T. Parasassi, G. De Stasio, R. Rusch, E. Gratton, A photophysical model for diphenylhexatriene fluorescence decay in solvents and in phospholipid-vesicles. Biophys. J. 59(2), 466–475 (1991)

    Article  Google Scholar 

  52. T. Parasassi, E. Krasnowska, L. Bagatolli, E. Gratton, LAURDAN and PRODAN as polarity-sensitive fluorescent membrane probes. J. Fluoresc. 8(4), 365–373 (1998)

    Article  Google Scholar 

  53. V.A. Parsegian, R.P. Rand, R.C. Rau, Osmotic stress, crowding, preferential hydration, and binding: a comparison of perspectives. Proc. Natl. Acad. Sci. USA 97, 3987–3992 (2000)

    Article  ADS  Google Scholar 

  54. G. Pollack, Cells, Gels and the Engines of Life. (A New, Unifying Approach to Cell Function), 1st edn. (Ebner and Sons, Seattle, 2001)

    Google Scholar 

  55. A.K. Poulsen, F.R. Lauritsen, L.F. Olsen, Sustained glycolytic oscillations—no need for cyanide. FEMS Microbiol. Lett. 236(2), 261–266 (2004)

    Google Scholar 

  56. A.K. Poulsen, A.Z. Andersen, J.C. Brasen, A.M. Scharff-Poulsen, L.F. Olsen, Probing glycolytic and membrane potential oscillations in Saccharomyces cerevisiae. Biochemistry 47(28), 7477–7484 (2008)

    Article  Google Scholar 

  57. K. Reijenga et al., Control of glycolytic dynamics by hexose transport in Saccharomyces cerevisiae. Biophys. J. 80(2), 626–634 (2001)

    Article  ADS  Google Scholar 

  58. P. Richard, The rhythm of yeast. FEMS Microbiol. Rev. 27(4), 547–557 (2003)

    Article  Google Scholar 

  59. P. Richard, B. Teusink, M.B. Hemker, K. van Dam, H.V. Westerhoff, Sustained oscillations in free-energy state and hexose phosphates in yeast. Yeast 12(8), 731–740 (1996)

    Article  Google Scholar 

  60. P. Richter, J. Ross, Concentration oscillations and efficiency—glycolysis. Science 211(4483), 715–717 (1981)

    Article  ADS  Google Scholar 

  61. T.D. Schrøder, V.C. Özalp, A. Lunding, K.D. Jernshøj, L.F. Olsen, An experimental study of the regulation of glycolytic oscillations in yeast. FEBS J. 280(23), 6033–6044 (2013)

    Article  Google Scholar 

  62. W. Stroberg, S. Schnell, Do cellular condensates accelerate biochemical reactions? Lessons from microdroplet chemistry. Biophys. J. 115(1), 3–8 (2018)

    Article  ADS  Google Scholar 

  63. B. Teusink et al., Synchronized heat flux oscillations in yeast cell populations. J. Biol. Chem. 271(40), 24442–24448 (1996)

    Article  Google Scholar 

  64. H.S. Thoke et al., Tight coupling of metabolic oscillations and intracellular water dynamics in Saccharomyces cerevisiae. PLoS ONE 10(2), e0117308 (2015)

    Article  Google Scholar 

  65. H.S. Thoke, S. Thorsteinsson, R.P. Stock, L.A. Bagatolli, L.F. Olsen, The dynamics of intracellular water constrains glycolytic oscillations in Saccharomyces cerevisiae. Sci. Rep. 7, 16250 (2017)

    Article  ADS  Google Scholar 

  66. H.S. Thoke et al., Is a constant low-entropy process at the root of glycolytic oscillations? J. Biol. Phys. 44, 419–431 (2018)

    Article  Google Scholar 

  67. H.S. Thoke, L.A. Bagatolli, L.F. Olsen, Effect of macromolecular crowding on the kinetics of glycolytic enzymes and the behaviour of glycolysis in yeast. Integr. Biol. 10(10), 587–597 (2018)

    Article  Google Scholar 

  68. J. Thomson, Biological Effects of Deuterium (Macmillan, New York, 1963)

    Google Scholar 

  69. M. Tros et al., Picosecond orientational dynamics of water in living cells. Nat. Commun. 8, 904 (2017)

    Article  ADS  Google Scholar 

  70. G. Weber, F.J. Farris, Synthesis and spectral properties of a hydrophobic fluorescent probe: 6-propionyl-2-(dimethylamino)naphthalene. Biochemistry 18(14), 3075–3078 (1979)

    Article  Google Scholar 

  71. F.E. Yates, Homeokinetics/homeodynamics: a physical heuristic for life and complexity. Ecol. Psychol. 20(2), 148–179 (2008)

    Article  Google Scholar 

  72. L. Yenush, Potassium and sodium transport in yeast, in Yeast Membrane Transport, Advances in Experimental Medicine and Biology, ed. by J. Ramos, H. Sychrova, M. Kschischo, vol. 892 (2016), pp. 187–228

    Google Scholar 

  73. H. Yoo, E. Nagornyak, R. Das, A.D. Wexler, G.H. Pollack, Contraction-induced changes in hydrogen bonding of muscle hydration water. J. Phys. Chem. Lett. 5(6), 947–952 (2014)

    Article  Google Scholar 

  74. C.K. Ytting et al., Measurements of intracellular ATP provide new insight into the regulation of glycolysis in the yeast Saccharomyces cerevisiae. Integr Biol. 4(1), 99–107 (2012)

    Article  Google Scholar 

  75. S. Zimmerman, S. Trach, Estimation of macromolecule concentrations and excluded volume effects for the cytoplasm of Escherichia-coli. J. Mol. Biol. 222(3), 599–620 (1991)

    Article  Google Scholar 

Download references

Acknowledgements

The authors acknowledge the Danish Molecular Biomedical Imaging Centre (DaMBIC, University of Southern Denmark) for the use of the bioimaging facilities. LFO was supported by a grant from the Danish Council for Independent Research, Natural Sciences (DFF 4002-00465).

Author information

Authors and Affiliations

  1. PhyLife, Institute of Biochemistry and Molecular Biology, University of Southern Denmark, Campusvej 55, 5230, Odense M, Denmark

    Lars Folke Olsen & Anita Lunding

Authors
  1. Lars Folke Olsen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anita Lunding
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lars Folke Olsen .

Editor information

Editors and Affiliations

  1. Department of Physics, Lancaster University, Lancaster, UK

    Aneta Stefanovska

  2. Department of Physics, Lancaster University, Lancaster, UK

    Peter V. E. McClintock

Rights and permissions

Reprints and permissions

Copyright information

© 2021 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Olsen, L.F., Lunding, A. (2021). Oscillations in Yeast Glycolysis. In: Stefanovska, A., McClintock, P.V.E. (eds) Physics of Biological Oscillators. Understanding Complex Systems. Springer, Cham. https://doi.org/10.1007/978-3-030-59805-1_13

Download citation

Publish with us

Policies and ethics

Search

Navigation