MEMBRANES

Enhanced water permeability andtunable ion selectivity in subnanometercarbon nanotube porinsRamya H. Tunuguntla,1* Robert Y. Henley,1,2* Yun-Chiao Yao,1,3 Tuan Anh Pham,4

Meni Wanunu,2 Aleksandr Noy1,3†

Fast water transport through carbon nanotube pores has raised the possibility to use them inthe next generation of water treatment technologies. We report that water permeabilityin 0.8-nanometer-diameter carbon nanotube porins (CNTPs), which confine water down toa single-file chain, exceeds that of biological water transporters and of wider CNT poresby an order of magnitude. Intermolecular hydrogen-bond rearrangement, required for entryinto the nanotube, dominates the energy barrier and can be manipulated to enhancewater transport rates. CNTPs block anion transport, even at salinities that exceed seawaterlevels, and their ion selectivity can be tuned to configure them into switchable ionicdiodes. These properties make CNTPs a promising material for developing membraneseparation technologies.

Increasing demands for fresh water pose aglobal threat to sustainable development,resulting inwater scarcity for 4 billion people(1, 2). Current water purification technolo-gies (3) can benefit from the development

of membranes with specialized pores that mimichighly efficient and water selective biologicalproteins such as Aquaporin-1 (AQP1). The keystructural feature that enables efficient trans-port in AQP1 is its hydrophobic and narrow0.3-nm-diameter channel, which forces waterto translocate in a single-file arrangement (4).The limited success of efforts to create scalableAQP-based membranes (5) motivated researchersto develop bioinspired artificial water channels(6, 7 ). Computer simulations (8–10) and ex-perimental studies of water transport throughcarbon nanotubes (CNTs) with >1 nm diameters(11–13) reported enhanced water flux in thesechannels. However, these nanotubes have failedto match the transport efficiency of AQPs andshowed disappointing ion selectivity that vanishedat higher salinities (14).We investigatedwater and ion transport through

carbon nanotube porins (CNTPs), ~10-nm-longCNT segments that spontaneously insert into alipid membrane to form transmembrane chan-nels (15). We compared transport through narrow0.8-nm-diameter CNTPs (nCNTPs), which forcewater into a one-dimensional (1D) wire configu-ration, to transport throughwider 1.5-nm-diameterCNTPs (wCNTPs) that maintain a bulklike water

arrangement. We measured CNTP water perme-ability in a stopped-flow apparatus by exposinglarge unilamellar vesicles (LUVs) with CNTPsembedded in their walls (Fig. 1A) to a hypertonicbuffer solution containingpyranine osmolyte. Thischarged membrane-impermeable osmolyte is toolarge to enter nCNTPs and wCNTPs. Osmotic pres-sure inducedwater efflux, and the resulting vesicleshrinkage was observed as increased light scatter-ing from the sample (16) (Fig. 1, B and C) (see fig.S1 for controls). From this data, we extracted thetrue water permeability, Pw, of the vesicles over arange of applied osmotic pressures (fig. S2) [seethe supplementary materials (SM) for details ofthe analysis and controls (17)]. Addition of CNTPsto the membrane increased its permeability, withoverall water permeabilities increasing linearlywith CNTP concentration (fig. S3) for bothwCNTPsand nCNTPs. Single-channel CNTP permeabilities,PCNTP (Table 1), reached 5.9 ± 1.3 × 10−14 cm3/s and6.8± 1.4× 10−13 cm3/s for thewCNTPs andnCNTPs,respectively, with the permeability of nCNTPs ex-ceeding that of wCNTPs by a factor of 11 and thatof AQP1 by a factor of 6. nCNTP permeability alsoagrees closely with the value of 5.1 × 10−13 cm3/scalculated from molecular dynamics (MD) sim-ulations for CNT pores of the same diameter (9).To provide an unbiasedmicroscopic description

of water dynamics inside CNTPs, we performedfirst-principlesMD simulations based on densityfunctional theory (see SM for details). Whereasthe structure and hydrogen-bonding (H-bonding)pattern inside wCNTPs resembled bulk water(Fig. 2, A and B, and fig. S16), water in nCNTPsadopted a single-file configuration (Fig. 2C andfig. S16), with a 1D H-bonding pattern that wasakin to AQP channels (18).What contributes to thegreaterwater flux through

a nCNTP, as compared to an AQP1 channel, whenboth structures similarly confine water in singlefile? Pore-lining residues in aquaporins can do-nate or accept H bonds to incoming water mole-

cules; thus, transport rates are limited by kineticsof H-bond breakage, molecular reorientation, andH-bond reformation (19). In contrast, CNTPwalls,which cannot form H bonds, permit virtuallyunimpeded water flow (fig. S17) (9).When we repeated our measurements at pH

3.0, where the anionic carboxylate groups (COO–)on the CNTP rim became protonated, we observedsignificant increases in water flux (Fig. 1D andTable 1), with nCNTPs and wCNTPs showing five-fold and fourfold enhanced permeabilities. Thisbehavior parallels findings in a simulation studywhere additionof fourCOO–groups to the rimsof a1.1-nm-diameter CNT reduced thewater flux three-fold due to enhanced rim-water interactions (20).We also measured water transport rates in

CNTPs over a temperature range of 10° to 50°Cand extracted the corresponding activationenergies (Fig. 1, F and G, and fig. S6 for LUV andAQP-1 Arrhenius plots). The activation energy (Ea)penalty of 24.1 kcal/mol at pH 7.8 for nCNTPsdecreased twofold at pH 3.0, highlighting theimportance of rim-water interactions for transportefficiency. The remaining energy barrier at pH3.0 should then originate from the H-bondingconfiguration of water molecules as they tran-sition from bulk to single file inside the nCNTP.Our simulations show that the average numberof H bonds drops from 3.9 in the bulk to 1.8 insidethe nCNTP (Fig. 2D), which, given the singleH-bond energy of 5.1 kcal/mol (21), implies anenergy penalty of 10.7 kcal/mole, in excellentagreement with the value of 10.6 kcal/mole mea-sured at pH 3.0. Activation energy measurementsfor the wCNTPs did not show a large change uponrim neutralization (Fig. 1G), suggesting that rim-water interactions do not play a substantial role inwater transport through wider channels. The com-bination of highwater permeability and relativelylarge activation energy observed inCNTPs suggestsan important role for collective motion of watermolecules in the transport mechanism (9, 22).Compounds that either strengthen(kosmotropes)

or break down (chaotropes) the intermolecularH-bonding network in water (23) altered the per-meability of nCNTPs (Fig. 1E). In nCNTPs, additionof kosmotropic glucose and trehalose decreasedwater permeability 14- and 9.3-fold, while chao-tropic agents, polyethylene glycol (PEG4) and urea,increased it 2- and 1.6-fold, respectively. Therefore,weakening interactionsbetween water moleculesfacilitates their rearrangement into a single-fileconfiguration. In wCNTPs, chaotropes also en-hanced water permeability by 11-fold (PEG4) and13-fold (urea); however, equivalent concentra-tions of kosmotropes did not alter permeabilitiesin wCNTPs, possibly due to a less stringent H-bonding rearrangement requirement in thesewider pores. We also observed permeability en-hancements in the presence of chaotropic PEG4

at pH 3 (fig. S5), indicating that the enhance-mentmechanism is not related to the chaotropeinteractions with the CNTP rim.We calculated the effective water diffusion co-

efficients, Dw, in CNTPs from their osmotic per-meabilities (Table 1) (see SM for details). Tominimize contribution from rim interactions, we

RESEARCH

Tunuguntla et al., Science 357, 792–796 (2017) 25 August 2017 1 of 5

1Biology and Biotechnology Division, Physical and LifeSciences Directorate, Lawrence Livermore NationalLaboratory, Livermore, CA 94550, USA. 2PhysicsDepartment, Northeastern University, Boston, MA 02115,USA. 3School of Natural Sciences, University of CaliforniaMerced, Merced, CA 94343, USA. 4Materials ScienceDivision, Physical and Life Sciences Directorate, LawrenceLivermore National Laboratory, Livermore, CA 94550, USA.*These authors contributed equally to this work. †Correspondingauthor. Email: noy1@llnl.gov

on March 12, 2020

http://science.sciencem

ag.org/D

ownloaded from

Tunuguntla et al., Science 357, 792–796 (2017) 25 August 2017 2 of 5

Fig. 1. Water transport through CNTPs. (A) A cartoon showing an LUVwith embedded CNTPs (not to scale). (Inset) Water molecules escapethe interior of the LUV through the CNTP to relieve an applied osmoticgradient. (B and C) Light-scattering traces recorded after subjectinglipid vesicles containing 1.5 nm wCNTPs (B), and 0.8 nm nCNTPs (C) tovarying osmotic gradients. (D) Water permeability values (pyranineosmolyte, N = 5) measured for nCNTPs and wCNTPs at two pH values(blue and red bars) compared to the water permeability of AQP1 proteinmeasured at pH 7.8, and water permeability of nCNTPs measured (N = 3)at pH 7.8 with 0.6 M NaCl osmolyte (gray bar). Water permeability of AQP1

measured in our experiments, 1.19×10−13 cm3/s, matches the literaturevalues (31). nCNTP permeability measured using NaCl osmolyte is greaterthan values measured using pyranine because of the chaotropic natureof NaCl (32). (E) Water permeability of CNTPs measured at pH 7.8 in thepresence of 150 mM concentrations of chaotropes PEG and urea, as wellas kosmotropes glucose and trehalose (N = 3). Dashed lines are guidesto the eye that indicate permeability levels measured without additives.(F and G) Arrhenius plots of the water permeability for nCNTPs (F) andwCNTPs (G), with corresponding activation energies indicated on thegraph (N = 3).

Table 1. Measured water permeabilities (mean ± SD, N = 5), diffusion coefficients, and computed diffusion coefficients of individual nCNTP,wCNTP, and AQP1 protein.

Channel pH

Pore

diam.

(nm)

Pore

length

(nm)

Water permeability, Pw Diffusion coefficient, Dw

(cm3/s) (H2O molec/s)Experiment

(cm2/s)

Simulation

(cm2/s)

wCNTP 7.8 1.35 13.4 5.9 ± 1.3 × 10−14 1.9 × 109 5.5 ± 1.2 × 10−6 —.. .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ..

3.0 1.35 13.4 2.2 ± 0.05 × 10−13 7.3 × 109 2.1 ± 0.2 × 10−5 3.90 × 10−5.. .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .

nCNTP 7.8 0.68 10.6 6.8 ± 1.4 × 10−13 2.3 × 1010 8.9 ± 0.4 × 10−6 —.. .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ..

3.0 0.68 10.6 3.4 ± 0.04 × 10−12 1.1 × 1011 4.4 ± 0.2 × 10−5 1.13 × 10−4.. .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .

AQP1 7.0 0.28 2.24 1.17 × 10−13 (18) 3.9 × 109 (18) 1.5 × 10−6.. .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .

RESEARCH | REPORTon M

arch 12, 2020

http://science.sciencemag.org/

Dow

nloaded from

focused on the Dw values measured at pH 3. Dw

measured for thewCNTPs (2.1 ± 0.2 × 10−5 cm2/s)correlateswellwith thebulkvalueof 2.3× 10−5 cm2/s(24). The higher Dw measured in nCNTPs (4.4 ±0.2 × 10−5 cm2/s) is also close to the value predicted(19) for 0.8-nm-diameter CNTs (~3.5 × 10−5 cm2/s).We also compared our resultswithDwdetermined

from our simulations by fitting the computedmean square displacement (MSD) to the powerlaw form (Fig. 2E). These fits indicate that waterdiffusion mechanism in CNTPs deviates signif-icantly from Fickian type in the bulk, where thepower lawcoefficienta =1, andmore so innCNTPs,where a reaches the value of 1.81. Furthermore,

the fittedDw ratio of 2.9 (nCNTP:wCNTP) is in rea-sonable agreement with the ratio of 2.1 obtainedin our experiments, also consistent with a furtherreductionof thenumberofHbondswithinnCNTPs.To evaluate their ion selectivity, we measured

ion transport through individual nCNTPs using amodified suspended lipid bilayer platform (Fig. 3A,

Tunuguntla et al., Science 357, 792–796 (2017) 25 August 2017 3 of 5

Fig. 2. Hydrogen-bonding pattern and water dif-fusion in CNTPs. (A to C). First-principles MDsimulations showing different H-bonding patternsfor water in the bulk state (A) and CNTPs of differentdiameters [(B) and (C)]. (D) Histogram ofthe average number of H bonds in nCNTPs, wCNTPs,and bulk water determined from the simulations.Dashed lines represent Gaussian fits. (E) Meansquare displacement (MSD) of water moleculesinside CNTPs, determined from the simulations (seeSM). Dashed lines indicate least squares fits to apower law in the form of MSD = 2D × ta (33, 34).Fitted a values were 1.60 and 1.81, and D valueswere 3.9 × 10−5 cm2/s and 11.3 × 10−5 cm2/s, forwCNTPs and nCNTPs, respectively.

bulk water wCNTP nCNTP

500

400

300

200

100

0

MS

D (

Å2)

20151050

Time (ps)

wCNTP nCNTP

60

50

40

30

20

10

0

Pro

babi

lity

(%)

86420Number of hydrogen bonds

nCNTP wCNTP bulk water

100

80

60

40

20

0

Con

duct

ance

(pS

)

3.02.52.01.51.00.50.0[KCl] (M)

2

4

68

10

2

4

68

100C

ondu

ctan

ce (

pS)

40.01

2 40.1

2 41

2

[KCl] (M)

pH 7.5 pH 3.0

~1/2

~1-5

0

5

Cur

rent

(pA

)

-100 -50 0 50 100 Voltage (mV)

-40

0

40

Cur

rent

(nA

)

-100 100Voltage (mV)

Bare poreLipid bilayerCNTP

8

6

4

2

0

Cou

nts

200150100500Conductance (pS)

CNTPLipid bilayer

SiNx

Si

V

Cis

Trans

+

nCNTP

Fig. 3. Ionic conductance of individual nCNTPs. (A) Measurement setupshowing a nCNTP inserted into an ~200-nm-diameter patch of lipid bilayerspanning the aperture of a solid-state nanopore. (B) Current-voltagecharacteristics (I-V curves) measured for a bare nanopore (blue), nanoporesealed with lipid bilayer (black), and nanopore sealed with the lipid bilayercontaining a single CNTP (red). (C) Histogram of the conductance valuesmeasured for individual CNTPs (red bars) compared with values measured

for pure lipid bilayer seals (gray bars). (D) Conductance of individual nCNTPsmeasured over a range of KCl concentrations at pH 7.5 (red circles) and 3.0(blue diamonds) (N ≥ 3). Dashed lines indicate fits to a Michaelis-Mentenconductance model (pH 7.5 data) and to a linear conductance model (pH 3.0data). (Inset) Conductance data plotted on a logarithmic scale, with dashedlines indicating power law fits to the data. The fit at pH 7.5 is based onconcentrations at or below 0.2 M.

RESEARCH | REPORTon M

arch 12, 2020

http://science.sciencemag.org/

Dow

nloaded from

and figs. S7 to S10) in which we burst a vesiclecontaining single or multiple CNTPs onto an~200-nm-diameter silicon nitride nanopore (seeSM). Unitary nCNTP conductance of 69 ± 6 pSobserved in these experiments (Fig. 3, B and C)matches values that we observed by monitoringstepwise spontaneous nCNTP insertions into lipidbilayer (figs. S10 and S11). We then explored therelationship between nCNTP conductance andelectrolyte (KCl) concentration in bilayers con-taining multiple nCNTPs. At pH 7.5, nCNTP con-ductance increased monotonically up to 250 mM,thereafter beginning to saturate (Fig. 3D). Single-file biological ion channels display similar behav-ior, where interactions of ions with the chargedresidues lead toMichaelis-Menten–type ion trans-port kinetics (25). Similarly, formoderate-to-high

electrolyte concentrations, interactions of potas-sium ions with the anionic carboxylic groups onthe nCNTP rim result inMichaelis-Menten tran-sport kinetics (Fig. 3D). At low salt concentrations,we observed a C 1/2 dependence (Fig. 3D, inset)that is different from the C 1/3 scaling reportedfor larger 7- to 28-nm-diameter CNTs at low con-centrations (26), although similar to the C 1/2 de-pendence recently reported for very long 1.3- to1.5-nm-diameter CNTs (27).Reversal potentialmeasurements, inwhich both

sides of the nCNTP are exposed to different saltconcentrations, allowed us to determine nCNTPion selectivity. These measurements, performedat pH 7.5 (Fig. 4A) (see figs. S12 to S14 for con-trols), showed that nCNTPs almost exclusivelyconduct cations, with ~0.99 permselectivity, cor-

responding to K+:Cl– ion selectivity greater than184:1 at typical seawater salinity level of 0.6 M.Thus, in our CNTPs, the negatively charged rimscreate a “good co-ion (Cl–) exclusion” condition,which is expected to produce our reported C 1/2

conductance scaling (28). Furthermore, perm-selectivity measurements at different electrolyteconcentrations show that strong anion exclusionin nCNTPs persists at up to 1M salinity levels (Fig.4C andTable 2), only diminishing at very high saltconcentrations (~2 M), in contrast to previousstudies where ion selectivity of 1.6-nm-diameterCNTs begins to drop at ~30 mM ionic strength(14). This strong ion selectivity also allowed us touse osmotic pressure from 0.6MNaCl to inducewater transport in nCNTPs (Fig. 1D and fig. S4),underscoring the potential of these narrow nano-tubes for water desalination applications.We can explore the mechanism of ion selec-

tivity in nCNTPs further by measuring their ionconductance and permselectivity at pH 3.0, wherethe rims are uncharged (Fig. 3D). At pH3.0, nCNTPconductance did not exhibit saturation but re-mained proportional to ion concentration (Fig. 3D,inset), indicating the removal of the rate-limitingstep of counterion binding to the charged rim.Moreover, reversal potential measurements forthe nCNTPs (Fig. 4B) at pH 3.0 showed a weakpreference to anions over cations, in strong con-trast to our observations at pH 7.5 (Fig. 4C).Lastly, we exploited the nCNTP’s tunable ion

selectivity to demonstrate an ionic diode. When

Tunuguntla et al., Science 357, 792–796 (2017) 25 August 2017 4 of 5

-8

-6

-4

-2

0

2

4

Cur

rent

(pA

)

-200 -100 0 100 200Voltage (mV)

cis / trans pH 7.5 / pH 7.5 pH 3.0 / pH 7.5 pH 7.5 / pH 3.0

pH 7.5 pH 3.0

1.0

0.9

0.8

Per

mse

lect

ivity

3 1 0.5 0.1 0.05 0.02[KCl] (M)

2.01.51.00.5

Debye length (nm)

-1.0

-0.5

0.0

sea waterbrackish water

pH 7.5

pH 3.0

-20

-10

0

10

20C

urre

nt (

pA)

-100 -50 0 50 100Voltage (mV)

cis / trans 3M/1M KCl 1M/1M KCl 0.1M/1M KCl 0.01M/1M KCl

10

5

0

-5

-10

Cur

rent

(pA

)

-100 -50 0 50 100Voltage (mV)

cis / trans 3M/1M KCl 1M/1M KCl 0.1M/1M KCl 0.01M/1M KCl

Cl-K+

Cl-Cl-

+

pH 7.5pH 3.0

XCl-K+

Cl-

+

pH 7.5pH 3.0

K+

Cl-Cl-Cl-Cl-K+

Fig. 4. Ion selectivity in nCNTPs. (A and B) Asymmetric I-V curves fornCNTPs recorded at pH 7.5 (A) and 3.0 (B). Permselectivity valueswere estimated from the values of reversal potential, which is the fittedx-intercept for each curve. (C) Permselectivity values at pH 7.5 and 3.0plotted as a function of the Debye length for the KCl electrolyte in the highsalt chamber. Permselectivity values represent experiments (N ≥ 3) (seeTable 2), where the KCl concentration in the high salt chamber was held at a

fixed value (as plotted on the top axis), and the lower salt chamber washeld at values below half of the KCl concentration in the high salt chamber.Horizontal lines indicate typical salinity ranges for seawater and brackishwater. (D) I-V curves recorded in 0.1 M KCl, when opposite sides of thenCNTPs were exposed to pH 7.5 and 3.0, as indicated. Inset diagramsshow ion flux direction at positive and negative applied voltages in theasymmetric pH case.

Table 2. Permselectivities (mean ± SD) and corresponding ion selectivity ratios measured fornCNTPs at pH 7.5 and 3.0 at varying KCl concentrations.

[KCl]

pH 7.5 pH 3.0

PermselectivitySelectivity ratio

(K+/Cl–)Permselectivity

Selectivity ratio

(Cl–/K+)

3 M 0.826 ± 0.007 (N = 3) 10.2 –0.354 ± 0.022 (N = 3) 2.2.. .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. .

1 M 0.976 ± 0.026 (N = 13) 80 –0.617 ± 0.069 (N = 9) 4.9.. .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. .

0.6 M 0.989 ± 0.027 (N = 3) 184 –0.457 ± 0.067 (N = 3) 2.9.. .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. .

0.1 M 1.031 ± 0.037 (N = 11) 1 –0.836 ± 0.062 (N = 3) 15.. .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... .. ... ... .. ... ... .. ... ... .. .

RESEARCH | REPORTon M

arch 12, 2020

http://science.sciencemag.org/

Dow

nloaded from

both sides of the nCNTPwere exposed to 100mMKCl solutions at pH 7.5, we observed a resistor-like linear current-voltage (I-V ) characteristic(Fig. 4D). However, when one side of the bilayerwas acidified to pH 3.0, the nCNTP exhibited ahighly rectifying diode-like behavior that indi-cates unidirectional ion transport, similar to rec-tification behavior observed in CNT membranes(29). Switching the pHgradient direction reversedthe direction of the diode conduction (Fig. 4D).Transition between resistor and diode behaviorwas robust, could be switched repeatedly, andwas observed even in 1 M KCl (fig. S15), pointingto potential applications of nCNTPs in dynami-cally reconfigurable ionic circuits (30).Our results indicate that sub-nm confinement,

which forces water molecules into a single-chainconfiguration, plays a critical role in enablingultrafast water transport and selective ion tran-sport in narrow CNTPs. High water permeabilityand ion selectivity of these channels, even at highsalinity, coupled with the potential to tune theirtransport properties, present opportunities todevelop ultrapermeable membranes for waterpurification applications, industrial separations,or flexible reconfigurable nanofluidic circuits.

REFERENCES AND NOTES

1. M. M. Mekonnen, A. Y. Hoekstra, Sci. Adv. 2, e1500323 (2016).2. C. J. Vörösmarty, P. Green, J. Salisbury, R. B. Lammers,

Science 289, 284–288 (2000).

3. Y. X. Shen, P. O. Saboe, I. T. Sines, M. Erbakan, M. Kumar,J. Membr. Sci. 454, 359–381 (2014).

4. P. Agre et al., J. Physiol. 542, 3–16 (2002).5. C. Y. Tang, Y. Zhao, R. Wang, C. Helix-Nielsen, A. G. Fane,

Desalination 308, 34–40 (2013).6. Y. X. Shen et al., Proc. Natl. Acad. Sci. U.S.A. 112, 9810–9815 (2015).7. M. Barboiu, A. Gilles, Acc. Chem. Res. 46, 2814–2823 (2013).8. B. Corry, J. Phys. Chem. B 112, 1427–1434 (2008).9. G. Hummer, J. C. Rasaiah, J. P. Noworyta,Nature414, 188–190 (2001).10. S. Joseph, N. R. Aluru, Nano Lett. 8, 452–458 (2008).11. M. Majumder, N. Chopra, R. Andrews, B. J. Hinds, Nature 438,

44 (2005).12. J. K. Holt et al., Science 312, 1034–1037 (2006).13. E. Secchi et al., Nature 537, 210–213 (2016).14. F. Fornasiero et al., Proc. Natl. Acad. Sci. U.S.A. 105,

17250–17255 (2008).15. J. Geng et al., Nature 514, 612–615 (2014).16. A. Milon et al., Biochim. Biophys. Acta 859, 1–9 (1986).17. Materials and methods are available as supplementary materials.18. K. Murata et al., Nature 407, 599–605 (2000).19. A. Horner et al., Sci. Adv. 1, e1400083 (2015).20. B. Corry, Energy Environ. Sci. 4, 751–759 (2011).21. E. Schwegler, J. C. Grossman, F. Gygi, G. Galli, J. Chem. Phys.

121, 5400–5409 (2004).22. B. L. de Groot, H. Grubmüller, Science 294, 2353–2357 (2001).23. H. Uedaira, H. Uedaira, Cell. Mol. Biol. 47, 823–829 (2001).24. R. Mills, J. Phys. Chem. 77, 685–688 (1973).25. P. H. Nelson, J. Chem. Phys. 117, 11396–11403 (2002).26. E. Secchi, A. Niguès, L. Jubin, A. Siria, L. Bocquet, Phys.

Rev. Lett. 116, 154501 (2016).27. H. Amiri, K. L. Shepard, C. Nuckolls, R. Hernández Sánchez,

Nano Lett. 17, 1204–1211 (2017).28. P. M. Biesheuvel, M. Z. Bazant, Phys. Rev. E 94, 050601 (2016).29. J. Wu, X. Zhan, B. J. Hinds, Chem. Commun. (Camb.) 48,

7979–7981 (2012).30. P. Ramirez et al., RSC Advances 6, 54742–54746 (2016).31. M. L. Zeidel, S. V. Ambudkar, B. L. Smith, P. Agre, Biochemistry

31, 7436–7440 (1992).

32. D. J. Tobias, J. C. Hemminger, Science 319, 1197–1198(2008).

33. F. Zhu, E. Tajkhorshid, K. Schulten, Phys. Rev. Lett. 93, 224501(2004).

34. G. Soveral, C. Prista, T. F. Moura, M. C. Loureiro-Dias, Biol. Cell103, 35–54 (2011).

ACKNOWLEDGMENTS

We thank P. Waduge, Northeastern University, for fabrication of thesolid-state nanopore chips; Y. Zhang, Lawrence Livermore NationalLaboratory (LLNL) for help with graphics used in Figs. 1 and 3; andV. Freger, Technion, Israel, for helpful discussions. T.A.P acknowledgessupport from the Lawrence Fellowship Program. Computationalresources were provided by the LLNL Institutional Computing GrandChallenge Program. This work was supported by the U.S. Department ofEnergy, Office of Basic Energy Sciences, Division of Materials Sciencesand Engineering. Work at LLNL was performed under the auspicesof the U.S. Department of Energy under contract DE-AC52-07NA27344.Work at the Molecular Foundry at Lawrence Berkeley NationalLaboratory was supported by the Office of Science, Office of BasicEnergy Sciences, of the U.S. Department of Energy under contractDE-AC02-05CH11231. Solid-state nanopore fabrication at Northeasternwas funded by National Science Foundation (grant EFMA-1542707).A.N. is an inventor on U.S. Patent Application Ser. No. 15/503,983,submitted by Lawrence Livermore National Security, LLC, which coverscarbon nanotube porins. A.N. holds shares in Porifera, Inc., a companythat commercializes carbon nanotube membrane technology.

SUPPLEMENTARY MATERIALS

www.sciencemag.org/content/357/6353/792/suppl/DC1Materials and MethodsSupplementary TextFigs. S1 to S17Table S1References (35–68)

16 March 2017; accepted 11 July 201710.1126/science.aan2438

Tunuguntla et al., Science 357, 792–796 (2017) 25 August 2017 5 of 5

RESEARCH | REPORTon M

arch 12, 2020

http://science.sciencemag.org/

Dow

nloaded from

porinsEnhanced water permeability and tunable ion selectivity in subnanometer carbon nanotube

Ramya H. Tunuguntla, Robert Y. Henley, Yun-Chiao Yao, Tuan Anh Pham, Meni Wanunu and Aleksandr Noy

DOI: 10.1126/science.aan2438 (6353), 792-796.357Science 

, this issue p. 792; see also p. 753Scienceof the nanotube, the authors were able to alter the ion selectivity.was the tunable rearrangement of intermolecular hydrogen bonding. Furthermore, by changing the charges at the mouthaccelerated water flow compared with that observed in biological water transporters. A key factor in the transport rate

10-nm) fragments of CNTs embedded in lipid bilayer membranes. Strong confinement generated highly∼short (Siwy and Fornasiero). In contrast to previous studies, the authors focused on water and ion transport through relatively

thoroughly characterized molecular transport through narrow carbon nanotubes (CNTs) (see the Perspective byet al.Enhanced water transport occurs in a number of narrow pore channels, such as biological aquaporins. Tunuguntla

Go with the flow

ARTICLE TOOLS http://science.sciencemag.org/content/357/6353/792

MATERIALSSUPPLEMENTARY http://science.sciencemag.org/content/suppl/2017/08/24/357.6353.792.DC1

CONTENTRELATED

http://science.sciencemag.org/content/sci/359/6383/eaaq1241.fullhttp://science.sciencemag.org/content/sci/359/6383/eaap9173.fullhttp://science.sciencemag.org/content/sci/357/6353/753.full

REFERENCES

http://science.sciencemag.org/content/357/6353/792#BIBLThis article cites 65 articles, 12 of which you can access for free

PERMISSIONS http://www.sciencemag.org/help/reprints-and-permissions

Terms of ServiceUse of this article is subject to the

is a registered trademark of AAAS.ScienceScience, 1200 New York Avenue NW, Washington, DC 20005. The title (print ISSN 0036-8075; online ISSN 1095-9203) is published by the American Association for the Advancement ofScience

Science. No claim to original U.S. Government WorksCopyright © 2017 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of

on March 12, 2020

http://science.sciencem

ag.org/D

ownloaded from