Abstract
Previous work assumed that ATP synthase, the smallest known rotary motor in nature, operates at 100% efficiency. Calculations which arrive to this result assume that the water viscosity inside mitochondria is constant and corresponds to that of bulk water. In our opinion this assumption is not satisfactory for two reasons: (1) There is evidence that the water in mitochondria prevails to 100% as interfacial water. (2) Laboratory experiments which explore the properties of interfacial water suggest viscosities which exceed those of bulk water, specifically at hydrophilic interfaces. Here, we wish to suggest a physicochemical mechanism which assumes intramitochondrial water viscosity gradients and consistently explains two cellular responses: The decrease and increase in ATP synthesis in response to reactive oxygen species and non-destructive levels of near-infrared (NIR) laser light, respectively. The mechanism is derived from the results of a new experimental method, which combines the technique of nanoindentation with the modulation of interfacial water layers by laser irradiation. Results, including the elucidation of the principle of light-induced ATP production, are expected to have broad implications in all fields of medicine.
Highlights
Result would already be sufficient to challenge the utilization of the viscosity of bulk water in the models and simulations used to assess the efficiency of the mitochondrial nanomotor
From the premise that bursts of reactive oxygen species (ROS) will accentuate the hydrophilic nature of the intramitochondrial space, the most plausible answer is that ROS enhances hydrophilicity, and thereby the viscous friction between surfaces moving relative to each other
A raise in interfacial viscosity impacts the rotation of the mitochondrial nanomotor, for instance, under conditions of prolonged oxidative stress, which are inescapably present during in vitro experiments, it can be reasonably assumed that a reduction of potentially elevated viscosity levels will manifest itself in an increase in ATP production
Summary
Probing nanoscopic interfacial water layers by nanoindentation and NIR laser light. Here, we report on laboratory experiments focusing on nanoscopic interfacial water layers which prevail on hydrophilic surfaces and are confined in subnanometer gaps, and their light tunability. It seems reasonable to assume that the origin of the relatively low force required to penetrate the first 100 nanometers into the hydrophilic samples, as depicted, is a reduction of the viscous friction in the tip/cavity interface by the laser light. It is tempting to assume that the nanomotor efficiency (ATP productivity) can be tuned with biologically tolerated intensities of red to NIR laser light This perspective receives justification from the experimental side: Previously, it was reported that red laser light (632.8 nm (power 15 mW, fluence 5 J ∙ cm−2) changed the energy metabolism in mitochondria irradiated in vitro, and caused an increase in ATP synthesis. We feel justified to assume that the irradiation upregulates ATP turnover by reducing the viscosity of the nanoscopic interfacial water layers which seem to control the efficiency of the mitochondrial nanomotor. This aspect is of considerable biological interest and may lead to a shift in the paradigm of ATP synthesis
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