Dynamic Surface Tension Enhances the Stability of Nanobubbles in Xylem Sap

Abstract

Air seeded nanobubbles have recently been observed within tree sap under negative pressure. They are stabilized by an as yet unidentified process, although some embolize their vessels in extreme circumstances. Current literature suggests that a varying surface tension helps bubbles survive, but few direct measurements of this quantity have been made. Here, we present calculations of dynamic surface tension for two biologically relevant lipids using molecular dynamics simulations. We find that glycolipid monolayers resist expansion proportionally to the rate of expansion. Their surface tension increases with the tension applied, in a similar way to the viscosity of a non-Newtonian fluid. In contrast, a prototypical phospholipid was equally resistant to all applied tensions, suggesting that the fate of a given nanobubble is dependent on its surface composition. By incorporating our results into a Classical Nucleation Theory (CNT) framework, we predict nanobubble stability with respect to embolism. We find that the metastable radius of glycolipid coated nanobubbles is approximately 35 nm, and that embolism is in this case unlikely when the external pressure is less negative than –1.5 MPa.

Functional xylem characteristics associated with drought‐induced embolism in angiosperms

“…1). Yet, it is unclear how stable these surfactant‐coated nanobubbles are over time, and under which fluctuating conditions (variation in temperature, pressure, gas solubility of xylem sap, gas concentrations in the surrounding xylem tissue) these tiny gas bubbles may expand to form a large embolism (Ingram et al ., 2021; Box Fig. 1).…”

“…( 8) Surfactant-coated nanobubbles: tiny gas bubbles can be stable in xylem sap as long as they are coated with surfactants (green) and have a diameter below a critical threshold for a given pressure. The fate of these bubbles, their stability in plant xylem and potential link to embolism are largely unknown (Schenk et al, 2015(Schenk et al, , 2017Ingram et al, 2021). ( 9) Wettability of the inner conduit wall: inner conduit walls must be hydrophilic for an optimal solid-liquid interface (contact angle between water and conduit wall < 90°), while hydrophobic walls (contact angle > 90°) attract surface nanobubbles that may trigger embolism (Zwieniecki & Holbrook, 2000;McCully et al, 2014;Schenk et al, 2017;Brodersen et al, 2018New Phytologist (2022…”

“…Of particular interest are the polar lipids due to their insoluble nature and potent surface activity, resulting in a wide range of dynamic surface tension of xylem sap. As will be explained further in this review, these surface‐active molecules may play a major role in the stability of tiny gas bubbles in xylem sap under negative pressure, which secures the water transport system and makes it more resilient to drought‐induced embolism than traditionally thought (Schenk et al ., 2017, 2020; Yang et al ., 2020; Ingram et al ., 2021; Jansen et al ., 2022).…”

Addressing controversies in the xylem embolism resistance–vessel diameter relationship

“…Importantly, this applies to all the drivers of embolism formation depending on gas dynamics discussed above. If embolism formation, for instance, was driven predominantly by the expansion of nanobubbles that exceed a critical size (Schenk et al ., 2017; Park et al ., 2019; Ingram et al ., 2021), a single bubble exceeding this threshold size would be sufficient to cause the complete loss of functionality of the corresponding vessel. Similarly, if emboli spread predominantly via gas diffusion through pit membranes (Guan et al ., 2021), it would only take one large enough bubble coming out of solution, for example after a temperature increase (see fig.…”

Angiosperms follow a convex trade‐off to optimize hydraulic safety and efficiency

“…Previous research found no effect of dissolved gas on bubble nucleation above À10 MPa (Hemmingsen, 1977(Hemmingsen, , 2006, but that research did not account for conditions existing in xylem; (2) nanobubbles present in sap may rapidly expand, depending on the pressure and gas concentration. This process would likely depend on the nature of the surfactant layer, such as the composition of polar lipids (Ingram et al, 2021). Regardless of the mechanism of embolism initiation, the fact that embolism propagation can temporarily degas the sap in the surrounding vessels and xylem tissue would delay initiation of further embolisms until the gas concentration locally reaches a certain threshold again.…”