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.
Similar content being viewed by others
References
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)
Goldbeter, A.: Biochemical Oscillations and Cellular Rhythms. Cambridge University Press, Cambridge (1996)
Richter, P.H., Ross, J.: Concentration oscillations and efficiency: glycolysis. Science 211(4483), 715–717 (1981)
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
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
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)
Lokta, A.J.: Contribution to the theory of periodic reactions. J. Phys. Chem. 14(3), 271–274 (1910)
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)
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
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
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
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
Ellis, R.J.: Macromolecular crowding: obvious but underappreciated. Trends Biochem. Sci. 26(10), 597–604 (2001)
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)
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
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
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)
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
Ling, G.N.: Nano-protoplasm: the ultimate unit of life. Physiol. Chem. Phys. Med. NMR 39(2), 111–234 (2007)
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
Onsager, L.: Reciprocal relations in irreversible processes I. Phys. Rev. 37, 405–426 (1931)
Onsager, L.: Reciprocal relations in irreversible processes II. Phys. Rev. 38, 2265–2279 (1931)
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
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)
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)
Kondepudi, D., Prigogine, I.: Modern Thermodynamics. From Heat Engines to Dissipative Structures. John Wiley & Sons Ltd,. Chichester (1998)
Einstein, A.: Theory of opalescence of homogenous liquids and liquid mixtures near critical conditions. Ann. Phys. 33, 1275–1298 (1910)
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
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
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
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
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
Bagatolli, L.A., Stock, R.P.: The cell as a gel: material for a conceptual discussion. Physiological Mini Reviews 9(5), 38–49 (2016)
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
Bockmann, M., Hess, B., Muller, S.C.: Temperature gradients traveling with chemical waves. Phys. Rev. E 53(5), 5498–5501 (1996)
Franck, U., Geiseler, W.: Zur periodischen Reaktion von Malonsäure mit Kaliumbromat in Gegenwart von Cer-Ionen. Naturwissenschaften 58, 52–53 (1971)
Franck, U.F.: Chemical Oscillations. Angewandte Chemie-International 17, 1–15 (1978)
Wang, T.: Studies on the action potential from a thermodynamic perspective. University of Copenhagen (2017)
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)
Schrödinger, E.: What is Life – the Physical Aspect of the Living Cell. Cambridge University Press (1944)
Ling, G.N.: Life at the cell and below cell level. The hidden history of a fundamental revolution in biology. Pacific Press, (2001)
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
Corresponding author
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
About this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10867-018-9499-2