Abstract
We detected very strong coupling between the oscillating concentration of ATP and the dynamics of intracellular water during glycolysis in Saccharomyces cerevisiae. Our results indicate that: i) dipolar relaxation of intracellular water is heterogeneous within the cell and different from dilute conditions, ii) water dipolar relaxation oscillates with glycolysis and in phase with ATP concentration, iii) this phenomenon is scale-invariant from the subcellular to the ensemble of synchronized cells and, iv) the periodicity of both glycolytic oscillations and dipolar relaxation are equally affected by D2O in a dose-dependent manner. These results offer a new insight into the coupling of an emergent intensive physicochemical property of the cell, i.e. cell-wide water dipolar relaxation, and a central metabolite (ATP) produced by a robustly oscillating metabolic process.
Highlights
The oscillatory behavior of many biological processes has been studied for decades
We focused on the phase relationships between fluorescence oscillations of the DAN probes and those of glycolytic metabolites, and perturbed the system with heavy water to quantify the response of the oscillators to determine the extent of coupling
In the experiments reported in this paper we focused on the two main fluorescent parameters of the DAN probes: i) emission intensity at a given wavelength, and ii) the Generalized Polarization function [21,27,28], which requires simultaneous measurement of two wavelengths
Summary
The oscillatory behavior of many biological processes has been studied for decades. Examples include slow genetic oscillations of circadian rhythms [1], periodic pattern formation in embryogenesis [2], oscillating cytoskeletal structure in mechano-sensitive hair bundles in the auditory system and, at the single cell level, the oscillations of Min gene products in Escherichia coli that dynamically determine the site of cell division, among others [3].The oscillatory nature of glycolysis in Saccharomyces cerevisiae becomes apparent when unmasked by inhibition of respiration. The oscillatory behavior of many biological processes has been studied for decades. Examples include slow genetic oscillations of circadian rhythms [1], periodic pattern formation in embryogenesis [2], oscillating cytoskeletal structure in mechano-sensitive hair bundles in the auditory system and, at the single cell level, the oscillations of Min gene products in Escherichia coli that dynamically determine the site of cell division, among others [3]. The oscillatory nature of glycolysis in Saccharomyces cerevisiae becomes apparent when unmasked by inhibition of respiration. As cells utilize glucose supplied in the medium, glycolysis products accumulate and disappear following a well-known waveform. Oscillations can be measured in real time following the intrinsic fluorescence of reduced nicotine adenine dinucleotide, NADH [4,5]. Oscillations of other intracellular glycolytic intermediates [6], CO2 [7], PLOS ONE | DOI:10.1371/journal.pone.0117308. Oscillations of other intracellular glycolytic intermediates [6], CO2 [7], PLOS ONE | DOI:10.1371/journal.pone.0117308 February 23, 2015
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