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. 2024 Sep 6;10(36):eado8081.
doi: 10.1126/sciadv.ado8081. Epub 2024 Sep 6.

Ion transport and ultra-efficient osmotic power generation in boron nitride nanotube porins

Zhongwu Li  1 , Alex T Hall  2 , Yaqing Wang  1 , Yuhao Li  1 , Dana O Byrne  3   4 , Lyndsey R Scammell  5 , R Roy Whitney  5 , Frances I Allen  4   6 , John Cumings  2 , Aleksandr Noy  1   7
Affiliations

Ion transport and ultra-efficient osmotic power generation in boron nitride nanotube porins

Zhongwu Li et al. Sci Adv. .

Abstract

Nanotube porins form transmembrane nanomaterial-derived scaffolds that mimic the geometry and functionality of biological membrane channels. We report synthesis, transport properties, and osmotic energy harvesting performance of another member of the nanotube porin family: boron nitride nanotube porins (BNNTPs). Cryo-transmission electron microscopy imaging, liposome transport assays, and DNA translocation experiments show that BNNTPs reconstitute into lipid membranes to form functional channels of ~2-nm diameter. Ion transport studies reveal ion conductance characteristics of individual BNNTPs, which show an unusual C1/4 scaling with ion concentration and pronounced pH sensitivity. Reversal potential measurements indicate that BNNTPs have strong cation selectivity at neutral pH, attributable to the high negative charge on the channel. BNNTPs also deliver very large power density up to 12 kW/m2 in the osmotic gradient transport experiments at neutral pH, surpassing that of other BNNT-based devices by two orders of magnitude under similar conditions. Our results suggest that BNNTPs are a promising platform for mass transport and osmotic power generation.

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Figures

Fig. 1.
Fig. 1.. Synthesis, characterization, and incorporation of BNNTPs.
(A) Schematic showing BNNTP preparation. i. Schematic of uncut BNNTs and a photograph of raw BNNTs in “puffball” status. ii. HIM imaging of dried BNNTs after dispersing with lipids in water and a photograph of uncut BNNT-lipids solution. iii. Schematic of cut, lipid-stabilized BNNT segments and a photograph of a cut BNNT suspension. iv. Schematic showing BNNTP incorporation into liposomes. (B) Histogram of the inner diameters of cut BNNT fragments measured with HR-TEM and a Gaussian fit to the data. Most BNNTPs show two to three walls. Inset: HR-TEM image of a single BNNTP. (C) Histogram of the lengths of the BNNTPs inserted into the lipid membrane and a Gaussian fit to the data. Inset: Cryo-TEM image of single BNNTP incorporated in the liposome bilayer (top) and individual BNNTPs (bottom). (D) Radius plot of the histogram of BNNTP tilt angles measured relative to the axis normal to the bilayer plane. (E) Time traces of the normalized fluorescence intensity of self-quenching CF dye after additions of BNNTPs to different concentrations. (F) Initial slopes of CF dye fluorescence intensity plotted as a function of BNNTP concentration. Dashed line is a linear fit to the data. Inset: Schematic illustration of CF dye leakage assay for qualitatively probing channel size formed by BNNTPs.
Fig. 2.
Fig. 2.. Ion transport in individual BNNTPs.
(A) Schematic illustration for single-channel recording of BNNTP conductance where an interface lipid bilayer formed between two droplets (top) and optical microscope image of hanging droplets with bilayer at the interface (bottom). (B) Representative conductance traces showing incorporation of BNNTPs into the lipid bilayer for 1 M KCl at pH 7.5. Control trace was recorded in absence of BNNTPs. (C) Histogram of BNNTP conductance values for 1 M KCl at pH 7.5. Dashed blue line is a Gaussian fit to the data. (D) Ion conductance of individual BNNTPs measured over a range of KCl concentrations at pH 7.5. Dashed line indicates fits to a power law. Inset: Ion conductivity versus KCl concentration for BNNTPs and bulk solutions (35) at pH 7.5. Dashed lines are best fits of the data to a power law. The ion conductivity of BNNTPs was determined from the ion conductance with κ=G4Lπd2+1d , where G is the conductance, L is the length, and d is the inner diameter of BNNTPs. (E) Ion conductance of individual BNNTPs measured over a range of pH for 1 M KCl. Dashed line is a guide to the eye.
Fig. 3.
Fig. 3.. DNA translocation through BNNTP ion channels.
(A) Schematic showing the translocation of ssDNA through a BNNTP in the lipid bilayer. Conductance trace showing multiple transient blockades caused by 50-nt ssDNA translocation through the BNNTPs with magnified view (bottom). The top trace shows the control recorded in absence of BNNTPs. (Buffer: 3 M KCl, pH 7.5). (B) Histogram of conductance blockade levels for ssDNA translocation events and the dashed blue line is a Gaussian fit to the data (left). Histogram of dwell times for ssDNA translocation events and the dashed blue line is a log-normal fit to the data (right). (C) Contour plots of the conductance blockade versus dwell time.
Fig. 4.
Fig. 4.. Ion selectivity and osmotic power generation in BNNTPs.
(A) I-V curves for different number of BNNTPs inserted into the membrane recorded for trans (1 M)/cis (0.1 M) KCl at pH 7.5. Inset: Schematic of the reversal potential measurements with asymmetric salt concentrations in two droplets. Transference number, permselectivity, and selectivity values were determined from the zero current potentials after subtracting the corresponding electrode redox potential. (B) K+ ion transference number and K+/Cl− ion permselectivity values at pH 7.5 plotted as a function of the Debye length for different KCl concentrations in the high-salt droplet. Dashed line is a guide to the eye. Inset, K+/Cl− ion selectivity values at pH 7.5 as a function of the KCl concentration. (C) K+ ion transference number and K+/Cl− ion permselectivity values plotted as a function of pH, where the KCl concentrations in the high-salt droplet and low-salt droplet are held at fixed values (1 M / 0.1 M KCl). Dashed blue line is best fit of K+ transference number to a pH titration function: t+=B0+B110−pKa 10−pH+10−pKa , where B0 and B1 are constants. (D) Osmotic power generation performance of BNNTPs compared with the reported larger BNNTs in terms of power density for different pH and salinity gradients. The power density values are calculated on the basis of power per unit pore surface area. The power density values of other larger BNNTs previously reported are taken from Siria et al. (15) (L ~ 1 μm, d = 80 nm), Pendse et al. (17) (L ~ 50 μm, d = 30 nm), and Cetindag et al. (18) (L ~ 5 μm, d = 3 nm, and d = 12 nm).
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