Extremophiles, microorganisms that thrive in extreme environments, have broadened our understanding of fundamental life processes. Cultivated strains of extremophiles have demonstrated the viability of life at temperatures up to 122 °C and pressures up to 125 MPa. These physical extremes affect intracellular mechanisms such as metabolism. At high temperatures, the key metabolite adenosine triphosphate (ATP) is subject to abiotic hydrolysis. In cells, ATP is complexed mostly with Mg2+. Although this complexation is well known, its role during abiotic ATP hydrolysis under extreme conditions has rarely been investigated.
This study presents novel kinetic data which are supported by thermodynamic modeling pertaining to ATP hydrolysis at elevated temperatures and 20 MPa in presence of Mg2+ and other cations. Kinetic parameters for abiotic hydrolysis were determined using in situ Raman spectroscopy in combination with a hydrothermal diamond anvil cell and a gas-pressurized autoclave equipped with a sapphire cell. Hydrolysis rate constants were studied using Mg2+, Ca2+, and Na+ as ATP counterions at temperatures of 80 °C, 100 °C, and 120 °C under pressures of 20 MPa. Our findings indicate that Na+ and Ca2+ ions have negligible effects on ATP hydrolysis rates. In contrast, increasing the Mg2+ concentration to fourfold the ATP concentration resulted in a pronounced decrease of the hydrolysis rate, with reductions of approximately 30 % at 80 °C and 50 % at 120 °C. By comparison with known biotic pool turnover rates, this kinetic stabilization of ATP reinforces previous findings that its abiotic hydrolysis is not a limiting factor for life at high temperature. Furthermore, these results suggest that Mg2+-rich intracellular compositions can reduce the energy investment required to maintain ATP homeostasis in biological systems. Thermodynamic modeling revealed increasing complexation of ATP with Mg2+ ions with increasing temperature and magnesium ions concentration. Under experimental conditions of pH 2 to 3, a continuous formation of MgH2ATP complexes was calculated, leading to a deceleration of the abiotic hydrolysis rate. At pH 6 to 9, the formation of MgATP2- was calculated at equimolar concentrations of ATP and Mg2+ ions. Above 80 °C and pH values between 6 and 9, thermodynamic modelling indicated the formation of Mg2ATP when the Mg2+ concentration was increased above the equimolar point.
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