Skip to main content
Log in

Is a constant low-entropy process at the root of glycolytic oscillations?

  • Original Paper
  • Published:
Journal of Biological Physics Aims and scope Submit manuscript

Abstract

We measured temporal oscillations in thermodynamic variables such as temperature, heat flux, and cellular volume in suspensions of non-dividing yeast cells which exhibit temporal glycolytic oscillations. Oscillations in these variables have the same frequency as oscillations in the activity of intracellular metabolites, suggesting strong coupling between them. These results can be interpreted in light of a recently proposed theoretical formalism in which isentropic thermodynamic systems can display coupled oscillations in all extensive and intensive variables, reminiscent of adiabatic waves. This interpretation suggests that oscillations may be a consequence of the requirement of living cells for a constant low-entropy state while simultaneously performing biochemical transformations, i.e., remaining metabolically active. This hypothesis, which is in line with the view of the cellular interior as a highly structured and near equilibrium system where energy inputs can be low and sustain regular oscillatory regimes, calls into question the notion that metabolic processes are essentially dissipative.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Duysens, L.N., Amesz, J.: Fluorescence spectrophotometry of reduced phosphopyridine nucleotide in intact cells in the near-ultraviolet and visible region. Biochim. Biophys. Acta 24(1), 19–26 (1957)

    Article  Google Scholar 

  2. Goldbeter, A.: Biochemical Oscillations and Cellular Rhythms. Cambridge University Press, Cambridge (1996)

    Book  MATH  Google Scholar 

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

    Article  ADS  Google Scholar 

  4. Chandra, F.A., Buzi, G., Doyle, J.C.: Glycolytic oscillations and limits on robust efficiency. Science 333(6039), 187–192 (2011). https://doi.org/10.1126/science.1200705

    Article  ADS  MathSciNet  MATH  Google Scholar 

  5. Cortassa, S., Aon, M.A., Westerhoff, H.V.: Linear nonequilibrium thermodynamics describes the dynamics of an autocatalytic system. Biophys. J. 60(4), 794–803 (1991). https://doi.org/10.1016/S0006-3495(91)82114-2

    Article  Google Scholar 

  6. Selkov, E.E.: Stabilization of energy charge, generation of oscillations and multiple steady states in energy metabolism as a result of purely stoichiometric regulation. Eur. J. Biochem. 59, 151–157 (1975)

    Article  Google Scholar 

  7. Lokta, A.J.: Contribution to the theory of periodic reactions. J. Phys. Chem. 14(3), 271–274 (1910)

    Google Scholar 

  8. Teusink, B., Larsson, C., Diderich, J., Richard, P., van Dam, K., Gustafsson, L., Westerhoff, H.V.: Synchronized heat flux oscillations in yeast cell populations. J. Biol. Chem. 271(40), 24442–24448 (1996)

    Article  Google Scholar 

  9. Thoke, H.S., Tobiesen, A., Brewer, J., Hansen, P.L., Stock, R.P., Olsen, L.F., Bagatolli, L.A.: Tight coupling of metabolic oscillations and intracellular water dynamics in Saccharomyces cerevisiae. PLoS One 10(2), e0117308 (2015). https://doi.org/10.1371/journal.pone.0117308

    Article  Google Scholar 

  10. Ytting, C.K., Fuglsang, A.T., Hiltunen, J.K., Kastaniotis, A.J., Ozalp, V.C., Nielsen, L.J., Olsen, L.F.: Measurements of intracellular ATP provide new insight into the regulation of glycolysis in the yeast Saccharomyces cerevisiae. Integr. Biol. (Camb) 4(1), 99–107 (2012). https://doi.org/10.1039/c1ib00108f

  11. Dodd, B.J.T., Kralj, J.M.: Live cell imaging reveals pH oscillations in Saccharomyces cerevisiae during metabolic transitions. Sci. Rep. 7(1), 13922 (2017). https://doi.org/10.1038/s41598-017-14382-0

    Article  ADS  Google Scholar 

  12. Thoke, H.S., Thorsteinsson, S., Stock, R.P., Bagatolli, L.A., Olsen, L.F.: The dynamics of intracellular water constrains glycolytic oscillations in Saccharomyces cerevisiae. Sci. Rep. 7(1), 16250 (2017). https://doi.org/10.1038/s41598-017-16442-x

    Article  ADS  Google Scholar 

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

    Article  Google Scholar 

  14. Zimmerman, S.B., Trach, S.O.: 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 

  15. Knull, H., Minton, A.P.: Structure within eukaryotic cytoplasm and its relationship to glycolytic metabolism. Cell Biochem. Funct. 14(4), 237–248 (1996). https://doi.org/10.1002/cbf.698

    Article  Google Scholar 

  16. Tros, M., Zheng, L., Hunger, J., Bonn, M., Bonn, D., Smits, G.J., Woutersen, S.: Picosecond orientational dynamics of water in living cells. Nat. Commun. 8(1), 904 (2017). https://doi.org/10.1038/s41467-017-00858-0

    Article  ADS  Google Scholar 

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

    Article  ADS  Google Scholar 

  18. Fels, J., Orlov, S.N., Grygorczyk, R.: The hydrogel nature of mammalian cytoplasm contributes to osmosensing and extracellular pH sensing. Biophys. J. 96(10), 4276–4285 (2009). https://doi.org/10.1016/j.bpj.2009.02.038

    Article  ADS  Google Scholar 

  19. Ling, G.N.: Nano-protoplasm: the ultimate unit of life. Physiol. Chem. Phys. Med. NMR 39(2), 111–234 (2007)

    MathSciNet  Google Scholar 

  20. Lu, C., Prada-Gracia, D., Rao, F.: Structure and dynamics of water in crowded environments slows down peptide conformational changes. J. Chem. Phys. 141(4), 045101 (2014). https://doi.org/10.1063/1.4891465

    Article  ADS  Google Scholar 

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

    Article  ADS  MATH  Google Scholar 

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

    Article  ADS  MATH  Google Scholar 

  23. Heimburg, T.: Linear nonequilibrium thermodynamics of reversible periodic processes and chemical oscillations. Phys. Chem. Chem. Phys. 19(26), 17331–17341 (2017). https://doi.org/10.1039/c7cp02189e

    Article  Google Scholar 

  24. Ling, G.N.: A Physical Theory of the Living State: the Association-Induction Hypothesis. Blaisdell Publishing Co, A Division of Random House, Inc., New York (1962)

    Google Scholar 

  25. Jaeken, L., Matveev, V.V.: Coherent behaviour and the bound state of water and K+ imply another model of bioenergetics: negative entropy instead of high energy bonds. The Open Biochemistry Journal 6, 139–159 (2012)

  26. Kondepudi, D., Prigogine, I.: Modern Thermodynamics. From Heat Engines to Dissipative Structures. John Wiley & Sons Ltd,. Chichester (1998)

  27. Einstein, A.: Theory of opalescence of homogenous liquids and liquid mixtures near critical conditions. Ann. Phys. 33, 1275–1298 (1910)

    Article  Google Scholar 

  28. Poulsen, A.K., Lauritsen, F.R., Olsen, L.F.: Sustained glycolytic oscillations--no need for cyanide. FEMS Microbiol. Lett. 236(2), 261–266 (2004). https://doi.org/10.1016/j.femsle.2004.05.044

    Google Scholar 

  29. Schroder, T.D., Ozalp, V.C., Lunding, A., Jernshoj, K.D., Olsen, L.F.: An experimental study of the regulation of glycolytic oscillations in yeast. FEBS J. 280(23), 6033–6044 (2013). https://doi.org/10.1111/febs.12522

    Article  Google Scholar 

  30. De Monte, S., d'Ovidio, F., Dano, S., Sorensen, P.G.: Dynamical quorum sensing: population density encoded in cellular dynamics. Proc. Natl. Acad. Sci. U. S. A. 104(47), 18377–18381 (2007). https://doi.org/10.1073/pnas.0706089104

    Article  ADS  Google Scholar 

  31. Olsen, L.F., Andersen, A.Z., Lunding, A., Brasen, J.C., Poulsen, A.K.: Regulation of glycolytic oscillations by mitochondrial and plasma membrane H+-ATPases. Biophys. J. 96(9), 3850–3861 (2009). https://doi.org/10.1016/j.bpj.2009.02.026

    Article  ADS  Google Scholar 

  32. Richard, P., Teusink, B., Hemker, M.B., Van Dam, K., Westerhoff, H.V.: Sustained oscillations in free-energy state and hexose phosphates in yeast. Yeast 12(8), 731–740 (1996). https://doi.org/10.1002/(SICI)1097-0061(19960630)12:8<731::AID-YEA961>3.0.CO;2-Z

  33. Bagatolli, L.A., Stock, R.P.: The cell as a gel: material for a conceptual discussion. Physiological Mini Reviews 9(5), 38–49 (2016)

    Google Scholar 

  34. Yashin, V.V., Kuksenok, O., Dayal, P., Balazs, A.C.: Mechano-chemical oscillations and waves in reactive gels. Rep. Prog. Phys. 75(6), 066601 (2012). https://doi.org/10.1088/0034-4885/75/6/066601

    Article  ADS  Google Scholar 

  35. Bockmann, M., Hess, B., Muller, S.C.: Temperature gradients traveling with chemical waves. Phys. Rev. E 53(5), 5498–5501 (1996)

  36. Franck, U., Geiseler, W.: Zur periodischen Reaktion von Malonsäure mit Kaliumbromat in Gegenwart von Cer-Ionen. Naturwissenschaften 58, 52–53 (1971)

    Article  ADS  Google Scholar 

  37. Franck, U.F.: Chemical Oscillations. Angewandte Chemie-International 17, 1–15 (1978)

    Google Scholar 

  38. Wang, T.: Studies on the action potential from a thermodynamic perspective. University of Copenhagen (2017)

  39. Ritchie, J.M., Keynes, R.D.: The production and absorption of heat associated with electrical activity in nerve and electric organ. Q. Rev. Biophys. 18(4), 451–476 (1985)

    Article  Google Scholar 

  40. Schrödinger, E.: What is Life – the Physical Aspect of the Living Cell. Cambridge University Press (1944)

  41. Ling, G.N.: Life at the cell and below cell level. The hidden history of a fundamental revolution in biology. Pacific Press, (2001)

Download references

Acknowledgements

HST and LFO thank the Danish Council for Independent Research|Natural Sciences for support. LAB is a member of the Argentinian Research Council (CONICET) research career. The authors thank Anita Lunding for skilled technical assistance.

Funding

This study was funded by a grant from the Danish Council for Independent Research|Natural Sciences (grant # DFF - 4002-00465).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Luis A. Bagatolli.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Electronic supplementary material

ESM 1

(DOCX 311 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Thoke, H.S., Olsen, L.F., Duelund, L. et al. Is a constant low-entropy process at the root of glycolytic oscillations?. J Biol Phys 44, 419–431 (2018). https://doi.org/10.1007/s10867-018-9499-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10867-018-9499-2

Keywords

Navigation