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Cavitation in lipid bilayers poses strict negative pressure stability limit in biological liquids

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Schneck,  Emanuel
Emanuel Schneck, Biomaterialien, Max Planck Institute of Colloids and Interfaces, Max Planck Society;

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Citation

Kanduč, M., Schneck, E., Loche, P., Jansen, S., Schenk, H. J., & Netz, R. R. (2020). Cavitation in lipid bilayers poses strict negative pressure stability limit in biological liquids. Proceedings of the National Academy of Sciences of the United States of America, 117(20): 201917195, pp. 10733-10739. doi:10.1073/pnas.1917195117.


Cite as: http://hdl.handle.net/21.11116/0000-0006-4F85-C
Abstract
Numerous biological systems contain metastable liquids at considerable negative pressures. As a prominent example, plants use negative pressures to suck water from the soil into their leaves. A long-debated mystery is why the maximal negative pressures are approximately −100 bar. A ubiquitous ingredient of biological liquids is lipids. Combining atomistic simulations and kinetic modeling, we show that lipid bilayers lead to cavitation at negative pressures of about −100 bar over timescales of hours to days, whereas water with added salt or nonpolar gas stays stable over many years. Our findings show that the presence of lipid aggregates imposes an upper stability limit for the magnitude of negative pressures in biological liquids.Biological and technological processes that involve liquids under negative pressure are vulnerable to the formation of cavities. Maximal negative pressures found in plants are around −100 bar, even though cavitation in pure bulk water only occurs at much more negative pressures on the relevant timescales. Here, we investigate the influence of small solutes and lipid bilayers, both constituents of all biological liquids, on the formation of cavities under negative pressures. By combining molecular dynamics simulations with kinetic modeling, we quantify cavitation rates on biologically relevant length scales and timescales. We find that lipid bilayers, in contrast to small solutes, increase the rate of cavitation, which remains unproblematically low at the pressures found in most plants. Only when the negative pressures approach −100 bar does cavitation occur on biologically relevant timescales. Our results suggest that bilayer-based cavitation is what generally limits the magnitude of negative pressures in liquids that contain lipid bilayers.