Lipid-Coated Nanobubbles in Plants: History
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Contributor:
Stephen Ingram
,
Steven Jansen
,
H. Jochen Schenk

One of the more surprising occurrences of bulk nanobubbles is in the sap inside the vascular transport system of flowering plants, the xylem. In plants, nanobubbles are subjected to negative pressure in the water and to large pressure fluctuations, sometimes encompassing pressure changes of several MPa over the course of a single day, as well as wide temperature fluctuations.

  • nanobubbles
  • polar lipids
  • plants
  • xylem

1. Introduction

When first proposed [1], the idea that nanobubbles could exist in sap in the vascular systems of plants was quite controversial. There was much debate among scientists as to whether gas nanobubbles could be stable in a bulk solution of water under constant atmospheric pressure, because high internal gas pressure in nanobubbles caused by surface tension would drive the gas into solution and dissolve the bubbles [2][3][4] unless the surrounding water were already super-saturated with gas. Despite this prediction, nanobubbles in aqueous bulk solution under atmospheric pressure have been found to be surprisingly stable [2][5][6][7][8]. There can be different reasons for this stability, including stabilization by electrostatic double layers at the air–water interface [7][9], stabilization involving hydroxyl ions [10] and electrolytes [11], diffusive shielding of bubble clusters in supersaturated water [12], and especially coating of nanobubbles with surfactant shells that reduce surface tension [4][13][14][15]. In all of the studies, stability of nanobubbles in bulk has been reported for water at or above atmospheric pressure. It may be even more surprising that bulk nanobubbles in water are found in the vascular system of plants, specifically the xylem, where they are subject to negative pressure in the water and large pressure fluctuations sometimes encompassing pressure changes of several MPa over the course of a single day.

2. What Is the Evidence for Nanobubbles in Plants?

Water in vascular plants, including angiosperms (the flowering plants, which make up 94% of all plant species), is transported in the xylem, a system of hollow dead conduits with rigid cell walls that connect roots, stems, leaves, and reproductive structures. Xylem is most noticeable as wood in woody plants. The water moving through xylem conduits is referred to as xylem sap. Xylem conduits include unicellular tracheids and multicellular vessels, and all conduits are connected to others via bordered pit pairs, where the sap on its way from one conduit to the next is forced to move through nanopores in so-called pit membranes, which largely consist of a mesh of cellulose microfibrils. Pit membranes are described below in the section addressing how nanobubbles form.
The existence of gas nanobubbles in xylem sap was first hypothesized based on observations of gas flow in wood. When a small hole was drilled into wood and gas flow was measured between the atmosphere and the wood, a net flow of gas into the wood was observed under most circumstances, peaking during the daytime, when sap flow rates are highest. This could not be caused by gas dissolving in sap, because xylem sap is normally gas-saturated or even super-saturated [16], and gas solubility decreases as temperatures increase during the day. Why, then, did gas move into the sap? Some of the researchers hypothesized that the gas moved into sap not by dissolving and not driven by a concentration gradient, but in the shape of gas nanobubbles driven by a pressure gradient [1]. This hypothesis spurred studies of nanobubble concentrations in xylem sap using nanoparticle tracking analysis (NTA) ([17]). While NTA does not distinguish between nanobubbles and other nanoparticles, it does allow qualitative assessment of whether the nanoparticles are spherical, which was the case for observations of nanoparticles in all ten flowering plant species whose xylem sap was analyzed using NTA. These included trees, shrubs, and a liana species, all of which contained nanoparticles in their sap ranging between 20 and 300 nm in radius [18][19] (Figure 1).
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Figure 1. Size distributions and concentrations of nanoparticles observed in eleven flowering plant species. Data taken from (a) [18] and (b) [19]. Differences in concentrations between the two datasets may be partly caused by the fact that during nanoparticle tracking analysis, the data in (a) were collected in moving samples while the data in (b) were from stationary samples.
To assess whether the nanoparticles in xylem sap were indeed nanobubbles, sap from two plant species, Geijera parviflora and Corylus avellana, was investigated using freeze-facture electron microscopy [18][19], resulting in images such as the one shown in Figure 2, where the spherical bubble shape is clearly visible in the facture plane along with remnants of the surfactant shells that coated the bubble.
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Figure 2. Freeze-fracture EM images of surfactant-coated nanobubbles in Geijera parviflora (A) and Corylus avellana (B). The gas bubble cores are visible as the white Pt/C free areas, while the dark Pt/C areas represent the surfactant coat, which can be chopped off, shifted, or wrinkled during the freeze-fracture preparation process. Scale bars = 100 nm.

3. What Is the Evidence for Polar Lipid Coatings of Nanobubbles in Xylem Sap?

The discovery that nanobubbles in xylem sap are coated by surfactant shells (Figure 2) was not a surprise, because uncoated nanobubbles would either shrink and dissolve or expand in response to the constant pressure and temperature changes inside a plant. However, this raised the further question of the chemical nature of these shells. Initial analyses of xylem sap residue found evidence both for polar lipids and proteins [18]. The former self-assemble in monolayers at water–gas interfaces, and the latter can be surface-active as well depending on their composition [20]. Polar lipids extracted from xylem sap of thirteen flowering plant species and analyzed via mass spectrometry [19][21] included both phospholipids and galactolipids, with a high proportion of phosphatidic acid (PA), a phospholipid with a negatively charged headgroup. Other charged phospholipids in xylem include negatively charged phosphatidylglycerol (PG), phosphatidylinositol (PI), and phosphatidylserine (PS), as well as zwitterionic phosphatidylcholine (PC) and phosphatidylethanolamine (PE). The amount of neutral galactolipids varied widely between species, making up between 7 and 75% of all polar lipids in xylem sap, and about 30% on average (Figure 3).
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Figure 3. Concentrations and chemical composition of polar lipids in xylem sap in twelve flowering plant species, including data from (a) California [21], and (b) Germany [19]. DGDG, digalactosyldiacylglycerol; MGDG, monogalactosyldiacylglycerol; PA, phosphatidic acid; PC, phosphatidylcholine; PE, phosphatidylethanolamine; PI, phosphatidylinositol; PS, phosphatidylserine. Figure modified from [21]. See Figure 1 for the full species names.
Polar lipids in xylem of flowering plants do not appear to change in concentration or composition seasonally [19][21] or over the lifetime of a plant. Comparison with the polar lipid composition of living xylem cells showed that the lipid composition is essentially the same in sap and living cells [21], suggesting that the lipids in dead conduits remain there after the rest of the living cell components have been enzymatically removed during the maturation of the conduit from a living cell into a dead hollow conduit.
It is not possible to separate polar lipids that coat nanobubbles in xylem sap from other polar lipids that coat other surfaces or form micelles in xylem; however, because polar lipids self-assemble at gas–water interfaces, it is clear that any polar lipids found in sap can be part of surfactant shells on gas nanobubbles. A significant correlation was found between the concentrations of nanoparticles and the concentrations of polar lipids in sap for three out of five species studied [19], further suggesting that surfactant shells on nanobubbles are made up largely of polar lipids. Proteins could contribute to these surfactant shells as well, including lipid transfer proteins that have surface-active properties and which are commonly found in xylem sap [22][23][24][25][26][27]. More research is needed to determine which proteins can be found in surfactant shells of xylem nanobubbles.

4. How Do Nanobubbles Form in Xylem?

Nanobubbles in xylem sap can only exist under the widely fluctuating pressure and temperature conditions experienced by plants if they are covered by surfactant shells. How do they form, though? As functioning xylem cannot be imaged at the nanoscale with currently available technology, there are no direct observations of nanobubbles forming in plants. There are two possibilities: (1) nanobubbles could form inside lipid micelles or lipid bilayers by diffusion of gas from sap through the lipids into the center of the micelles, which are occupied by the hydrophobic acyl chains of polar lipids and as such are largely hydrophobic and free of water [28]; or (2) gas could move into xylem sap via mass flow from other xylem compartments that contain a gas phase [1].
Option (1), diffusion of gas into the center of lipid micelles or bilayers, would only create a bubble if the resulting gas pressure counteracts the molecular forces that pull the lipids together, including hydrogen bonds between hydrophilic headgroups and relatively weak dispersion forces between the hydrophobic tails. Negative pressure in the surrounding sap could provide the necessary pull. However, molecular dynamics situations have shown that at the spatial and time scale applicable to plants, i.e., the volumes of conduits and the duration of negative pressure conditions, it would take on the order of −10 MPa of negative pressure in the sap to pull micelles or bilayers apart and create a void that could be occupied by gas [28]. Very few plant species ever reach −10 MPa of pressure in their xylem, and it could be that the instability of lipid bilayers and micelles under those conditions is the reason why plants cannot operate at more negative pressures [28]. When lipid bilayers are pulled apart under negative pressure the process is very unlikely to result in nanobubbles, because the energy released during this cavitation event would favor creation of a large cavitation void and thereby create a xylem embolism, i.e., fill the whole conduit with gas, rather than create a stable nanobubble. While it is unlikely that cavitation in lipid bilayers or micelles occurs within the normal pressure range in the xylem of most plants, which ranges between 0 and −5 MPa [29], it is important to realize that the probability of such events increases with the volume of xylem and with the duration and strength of negative pressure [28]. Therefore, xylem embolisms could occasionally form through this process.
Option (2), nanobubble formation from a preexisting gas phase such as an embolized conduit, is far more likely than option (1). Where an embolized (i.e., gas-filled) xylem conduit borders on another one, the gas and liquid phases are separated by mesoporous pit membranes. The discussion here addresses flowering plants, not conifers, which have a very different pit membrane morphology [30]. In flowering plants, these are fibrous membranes ranging in thickness from less than 200 to more than 900 nm [31], largely consisting of aggregated cellulose microfibrils that are between 20 and 30 nm thick [32]. Pores through such fibrous membranes have numerous pore constrictions or pore throats, with thicker membranes having a longer pore pathway and more pore constrictions [32]. The largest constriction size tends to be about 20 nm in diameter [33]. If nanobubbles form in pit membranes between gas-filled and sap-filled conduits, than they would have to form by gas overcoming the surface tension and moving through these constrictions (Figure 4).
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Figure 4. Diagram of nanobubbles forming in a pit membrane of a bordered pit between adjacent conduits. Lipid-coated nanobubbles are formed by a snap-off event due to the presence of surface-active lipids and pore constrictions between cellulose microfibrils. In addition to surfactant-coated nanobubbles, this image shows a wide range of nanoparticle sizes, which can be bilayer to multilayer micelles and vesicles associated with pit membranes. Reprinted with permission from Ref. [21].
According to the Young–Laplace equation, the pressure difference forcing a bubble through a 20 nm pore, assuming a contact angle of zero [34][35] and a pore shape correction factor of 0.5 to account for the fact that pores in fibrous membranes are not cylindrical [1], would be 7.2 MPa, assuming surface tension of pure water of 72 mJ m−2. Pit membranes are coated with polar lipids [18][36][37], which reduce the surface tension to about a third of pure water if the polar lipids are in equilibrium [38][39]. At a surface tension of 24 mJ m−2, a meniscus could pass through a 20 nm pore with a shape correction factor of 0.5 under a pressure difference between the gas and liquid phase of 2.4 MPa [33]. If pores are slightly larger than 20 nm or surface tension is slightly lower, then the pressure difference required for gas movement through a pore constriction would be even lower. Such pressure differences are well within the range of pressures experienced in the xylem of many plant species [29].
Movement of a meniscus through a pore constriction would not result in a continuous stream of gas from the gas into the liquid phase, instead resulting in snap-off of a nanobubble inside the membrane if the radius of the constriction were less than half the radius of the pore behind it [40][41], which would be the case in fibrous membranes. In geometrically complex pore spaces, the invasion of a non-wetting fluid, such as gas invading a pit membrane wetted with water, occurs not as a simple wetting front, but in rapid snap-off events and so-called Haines jumps [42][43]. Second, the entry of gas into the liquid phase increases the local liquid pressure, which causes bubble snap-off at the pore constriction. Due to the low compressibility of liquid water, the pressure release caused by bubble entry into water under negative pressure is substantial; a bubble that compresses water volume in the confined space within a pit border (around 0.5 to 10 μm3 [44]) by only 0.1% releases about 2 MPa of negative pressure [1][45][46]. Third, in liquid that is under negative pressure, minimization of the surface area created by formation of a single small bubble is always thermodynamically favored over rupture of hydrogen bonds between water molecules at the gas–water interface, which requires far more tensile energy density [47]. Therefore, movement of gas through nano-sized pore constrictions under negative pressure initially would produce nanobubbles, not a continuous stream of gas or a cavitation void. Thus, the multiphase interactions between gas, xylem sap, mesoporous pit membranes, and surfactants lead to surfactant-coated nanobubbles.
The pores in pit membranes play another important role for the persistence of nanobubbles in xylem conduits, as they are too small to allow passage of lipid-coated nanoparticles or most lipid micelles (see Figure 1). Therefore, nanobubbles do not move with the sap from one conduit to another or into living cells, and do not accumulate in leaves, instead remaining locked inside individual xylem conduits [19].
The scenario described here for nanobubble creation in pore constrictions depends on the presence of polar lipids inside the pore, lowering the surface tension. Without polar lipids, it would take a far higher pressure difference to force a meniscus through. If polar lipids are present in the pores, then they would invariably coat the nanobubbles because of the strong surface activity of polar lipids. Considering the normal pressures in xylem, the sizes of pore constrictions in pit membranes, and the presence of polar lipids in pit membranes, it appears inevitable that lipid-coated nanobubbles will form in pit membranes that separate gas-filled and sap-filled xylem conduits. The question then arises as to how such bubbles can possibly be stable under the physical conditions that exist in xylem.

This entry is adapted from the peer-reviewed paper 10.3390/nano13111776

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