Ion Transport in Nanofluidic Devices for Energy Harvesting

Review

Ion Transport in Nanofluidic Devices for Energy Harvesting Kai Xiao,1,* Lei Jiang,2 and Markus Antonietti1

Our technological systems are mainly based on semiconductor photovoltaics, electronic circuits, and (electro)chemical storage reactions. However, in the energy field, ‘‘ionics’’ has the potential to complement ‘‘electronics.’’ The control of ion transport is a necessary condition for the existence of life, e.g., both the energy conversion into ATP and the energy consumption to regulate biological functions occurs via directed ion or proton transport. These processes can be mimicked in synthetic devices and (nano)machines and then used for energy harvesting. This review will discuss and summarize the state of the art in the field of ion-transport-based energy conversion systems including ion passive transport for salinity gradient energy conversion and ion active transport for solar energy harvesting and then venture to propose several potential strategies to construct ion transport (passive or active) systems for energy conversion and storage devices, which are useful to drive local chemical reactions or electric current generation. Introduction One of the key challenges faced by our modern society and humans is sustainable, abundant, and inexpensive sources of clean energy.1 Both solar energy and salinity gradient energy (the latter named ‘‘blue energy’’) are such sources and in principle easy to harvest. It has been estimated that around 3,400,000 EJ solar energy reaches Earth every year, which exceeds by far humankind’s needs.2 Salinity gradient energy is indirectly related to solar energy (by water evaporation) and is stored as the salinity difference between seawater and freshwater. Based on the entropy change associated with saltwater mixing, it is estimated that 0.8 kWh m 3 can be produced at the sea-river interface.3 Although the involved energy density is typically 4–5 orders of magnitude lower than that contained in chemical energy of fossil fuel, the sheer amount of available fresh and salty water (for instance at the Yangtze river muzzle) makes this energy source very appealing. Currently, several approaches including pressure-retarded osmosis (PRO)4 and conventional reverse electrodialysis (RED)5 have been proposed to harvest energy from this salinity gradient, but a larger-scale application is still restricted by low performance, high cost, membrane fouling, and thereby viability. Therefore, boosting energy-harvesting efficiency is a scientific challenge but is also of general significance to solve the energy sustainability problem. Nature, however, can provide a unique perspective on ‘‘ionic power’’ for us because energy conversion and storage systems in biology work via ion transport and energy storage molecules, working hand by hand in an integrative and effective way. Two different ion transport modes, including ion passive transport and ion active transport, are widely used by organisms for harvesting and storing energy. The electric eel is a system optimized by evolution for power generation from ionic gradients. By using thousands of membranes with densely packed and highly selective ion channels, electric eels can generate large transient voltage and current with a

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Context & Scale Access to sustainable clean energy is one of the key challenges faced by our modern society. Although several sources of clean energy including solar, wind, and water power have been identified and developed, to date, none of these power sources can replace fossil fuels, mainly because of the limited efficiency and high cost of generating and storing electrical power. Nature can perhaps provide a unique perspective for clean energy generation because energy conversion and storage systems in biology work via ion transport and energy storage molecules in an integrative and effective way. The recent development of iontransport-based energy conversion systems has attracted more and more attention. The ion passive transport for salinity gradient energy generation has realized power density of approximately 5 W m 2, which has been flagged as the target for making salinity gradient power economically viable. Meanwhile, ion active transport has enough ‘‘power’’ to pump ions against steep concentration gradients up to 5,000-fold and can be used for photoelectric energy conversion. Taking the long view, these iontransport-based energyharvesting systems should be considered as a primary method,

discharge power of 100 W, entirely from the flux of small ions.6 A typical example of an active ion-transport-related biological process is the operation mode of bacteriorhodopsin (a type of photoprotein), which exists in the cell membrane and can pump protons from low to high concentration to create an electrochemical osmotic potential, which is later used to drive a molecular machine to produce ATP.7 The ion-transport-based energy-harvesting systems in biological organisms are smart and efficient. The question is whether we can harvest energy by ion transport like nature or even in ways exceeding nature? The answer is yes, as technology is able to use a much broader materials base, all operating via ion transport in nanofluidic entities.8 Ion transport in nanofluidics is a reasonably young research field, which benefits from the recent developments in synthesis techniques for organic and inorganic materials allowing pore diameter and length to be controlled in the nanometer range.9 Taking inspiration from diverse biological ion channels, various types of nanopores, nanochannels, and nanopipettes within different materials and with different morphologies have been synthesized by different techniques10 and were used to study fundamental ion transport functions, e.g., ion selectivity, ion rectification, and ion pump properties, among other examples.11 Beyond that, various engineering applications of ion transport in nanofluidics have been explored, such as sensing, ultrafiltration, desalination, and energy conversion and storage.12,13 In terms of energy conversion, ion-transport-based systems hold several advantages compared to electrons transport systems, e.g., safe and reliable energy devices and simple energy conversion processes based on abundant resources. On the other hand, ion-transport-based energy-harvesting systems still meet the disadvantages of low energy efficiency and poor power density so far. However, ion transport for energy harvesting is just an emerging and rather unexplored topic at the interface between membrane science, materials chemistry, and nanoscale fluid dynamics. Beyond that, the theoretical numerical predictions for potential improvements are very high. Ahead of a practical exploration or even industrial processes, it is still required to understand, optimize, and simplify such energy conversion process and device. Taking the long view, ions transport-based energy-harvesting system should be considered as an efficient supplementary way for clean energy harvesting,3 especially for small portable power supplies.

or at least an efficient supplementary way for clean energy harvesting. In this review, we mainly focus on ion-transport-based energy conversion. Aiming to get a deeper understanding of iontransport-based energy conversion systems, the operating mechanisms, including ion selectivity and ion rectification, are discussed first. For the ion passive transport for harvesting salinity gradient energy, the specific features and power density of 1D/2D/3D nanofluidics are summarized. For the ion active transport for solar energy generation, three preliminary approaches and their derived concepts, including pseudo-ion pump/physical ion pump/ chemical ion pump, are proposed. Finally, future ion transport energy-harvesting devices, opportunities, and challenges are speculated upon.

In this article, we present an overview of the ion transport in nanofluidic and its application in energy-harvesting system. We first introduce two important factors, ion selectivity and ion rectification, that affect ion-transport-based energy harvesting. Then, we mainly present recently developed ion-transport-based energy-harvesting systems: one group is based on ion passive transport for salinity gradient energy harvesting; another type is based on ion active transport for direct solar energy conversion. Finally, some predicted conceptually new, ion-transport-based, integrative devices are discussed. Ion Selectivity An elemental issue is to understand the separation of cations from anions in a charged nanofluidic device. In surface-charged nanofluidic channels, the counterions preferentially transport over the co-ions, known as ion selectivity, which works via the electrical double layers (EDL). At the charged wall, electrostatic force repels ions with the same charge as the wall (co-ions) and attracts ions with the opposite charge (counter-ions).14 However, only a fraction of counter-ions end up at the charged wall. Thermal energy and Boltzmann distribution create the graded EDL

1Max

Planck Institute of Colloids and Interfaces, Department of Colloid Chemistry, 14476 Potsdam, Germany

2Key

Laboratory of Bio-inspired Materials and Interfacial Science, Technical Institute of Physics and Chemistry, Chinese Academy of Sciences, Beijing 100190, P.R. China *Correspondence: [email protected] https://doi.org/10.1016/j.joule.2019.09.005

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Figure 1. Basic Principle of Ion Transport in Nanofluidics (A) Schematic diagram of the electrical double layer mechanism (EDL) next to a negatively charged wall. (B) Electrical distribution from charged wall to bulk solution. (C) Ion selectivity in a surface-charged nanochannel. The electrical double layers (Stern layer and diffusion layer) near the surface are overlapped when the diameter of the nanochannel is comparable with Debye length, and then the co-ions are excluded from the channel, while counter-ions can pass through the channel smoothly. (D) Steaming current induced by a pressure drop. PHigh , high pressure; PLow, low pressure. (E) Net diffusion current induced by salt concentration difference. C High , high concentration; C Low, low concentration. (F) Diffusion-osmotic current induced by salt concentration difference. (G) Ion rectification in an asymmetric charged nanochannel. The ion pass through the channel with a preferential direction, while it is suppressed in another direction when the nanochannel or membrane is asymmetric in structure or (and) surface charge. (H) Ion passive transport from high concentration to low concentration, corresponding to ion channel in biological system. (I) Ion active transport from low concentration to high concentration, corresponding to ion pump in biological system.

adjacent to the wall, with an increased concentration of counter-ions and a decreased concentration of co-ions (Figure 1A). The notation EDL refers to the first Stern layer and the second diffusion layer.15–17 The Stern layer is comprised entirely of counter-ions due to contact interactions. The diffusion layer is the region from the Stern layer to the bulk solution, where the distribution of free ions is still modified by the Coulomb force, electrically screened by the Stern layer. The EDL is usually simplified by an exponentially decaying potential between the surface and any point in the electrolyte solution (Figure 1B). The characteristic length of this area is the Debye

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screening length (l), which varies with the ionic strength, I, as lfI 1/2.9 In a nanochannel with dimensions similar to the Debye screening length,9 the EDLs of opposite sited overlap, by which way the channel is filled with a close to unipolar solution of counter-ions, and ion selectivity of transport can be observed (Figure 1C). Based on the ion-selectivity mechanism, electrokinetic energy can be harvested in two modes in a nanofluidic system: the streaming current18,19 and the net diffusion current.20 A streaming current is generated when the ionic solution is propelled through charged nanofluidic channels by an external mechanical driving force (Figure 1D). In this way, the hydraulic flow will drag the net charges (the counter-ions) within the EDL to move with velocity V. Streaming currents along charged surfaces is a part of electrokinetic phenomena,21 which has a rich history of several decades and has been well studied.19,22 A net diffusion current (Figure 1E) is generated from the separation of cations from anions within the EDL under a transmembrane concentration difference. In this case, the counter-ions spontaneously and preferentially diffuse along nanochannels with overlapping EDL and without the assistance of an externally applied electrical voltage or mechanical driving force. In this way, a transmembrane potential is built up, which is the ‘‘inversion’’ of the phenomena occurring in a supercapacitor. It is worth mentioning that diffusion-osmotic transport (Figure 1F), which was introduced by Derjaguin in the 1940s, is also raising interest recently.3,23,24 Diffusionosmosis is generated because the salt concentration difference builds an osmotic pressure gradient within the diffuse layer at the interfaces24,25; therefore, it is a combined process based on diffusion and osmosis. The advantage of diffusion-osmosis is that it does not require membrane semi-permeability or full ionic selectivity to generate an electric current and therefore allows the use of much larger pore to decrease impedance or increase ionic flux. Ion Rectification Ion rectification is a unique effect observed in nanofluidic devices and has been well studied in the last two decades.26–29 For a nanofluidic rectifier, the current recorded for one voltage polarity is higher than that recorded for the same absolute value of voltage with opposite polarity, which indicates a diode-like transport characteristic with a preferential direction of ion flow (Figure 1G). Theoretical calculation confirms that ionic rectification results from the accumulation or depletion of ions in response to different bias polarities and is due to the asymmetric cation/anion ratios established by symmetry breaking in nanofluidic devices, such as asymmetric device structure or dissymmetry of the fluidic environment.26,30–33 This nonlinear ion transport is fundamentally appealing, as it can be of considerable practical value. For a nanofluidic or porous membrane exhibiting an ionic diode behavior, its resistance acts as known from a Shockley diode. Under reverse bias, the ionic diode suppresses the back current, which is equivalent to increase membrane resistance (Rm) in the reverse bias configuration. When the nanofluidic ionic diode is in contact with a load resistance (RL) associated with the device used to extract the generated power, the generated current Iosm mainly flows and dissipates through the load resistance because of the much larger membrane resistance (Rm) than RL. In this way, the ionic diode will avoid power dissipation in the nanofluidic device itself as joule heating, and power density (P) can be boosted effectively by P = Iosm2RL.34 By the principle of ion selectivity and ion rectification, both the ions transport following a concentration gradient and against a concentration gradient can be used for energy harvesting. Ion transport from high concentration to low

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concentration is a passive transport process and can be mainly used for harvesting so called ‘‘blue energy’’ from existing salinity gradient (Figure 1H). In contrast, ion transport from low concentration to high concentration is an active transport process to harvest and store energy, called ion pump (Figure 1I). Ion Passive Transport for Salinity Gradient Energy Conversion The ion passive transport across a nanofluidic structure for salinity gradient energy harvesting is rather new and called nanofluidic reverse-electrodialysis (NRED) method.8 Compared to conventional PRO or RED with sub-nanometer porous semipermeable membranes, the current density and energy conversion efficiency in a NRED can be improved because of the larger pore size involved in the nanofluidic device. In NRED, the net diffusion current is generated from the unidirectional movement of one ionic component when salt concentrations in the two sides of a nanofluidic are different. In this section, we discuss the development of NRED systems from the fundamental mechanistic studies in 1D nanofluidic channels to the application studies of 2D layered membranes and 3D porous membranes. 1D single nanopores, nanochannels, and nanotubes are the suitable objects to study the principle of salinity gradient energy conversion because their geometry and chemistry can be well controlled and engineered (Figure 2A).33,35 An external mechanical driving force has been used to propel ionic solution to generate a streaming current for many years.36 For example, Daiguji22,37 and Dekker18,19 have reported the generation of streaming current through charged 1D nanofluidic channels by pressure-driven liquid flow. Ren et al.38 investigated theoretically the influence of hydrodynamic slip at the surface of channel on the energy conversion efficiency. In recent decades, more and more attention is provided to apply a salinity difference, which can drive ions transport across nanofluidic to generate a net diffusion current and a membrane potential. An ion-track-etched polyimide conical nanochannel was the first example to be used for harvesting salinity gradient energy by 1D nanofluidics.20 In this work, a maximum power out of Pmax z 26 pW per channel (8.3 W/m2) with an efficiency of 22.1% was obtained. In fact, the power density can be effectively regulated by adjusting external conditions, including the ion diffusion direction, pH of the electrolyte, and concentration ratio on the two sides. For example, theoretical calculation showed that a power density of 18.2 W/m2 could be realized by regulating the pH of electrolyte for the signal conical nanochannel NRED system.39 The underlying principle for all these external conditions is to increase the pore surface charge density. For example, a power density up to 4,000 W/m2 from a 1,000-fold salinity gradient was reported for a single boron nitride (BN) nanotube.23 In this work, an ultrahigh surface charge density up to 1 C/m2 has a key influence on this high power density. Different from streaming current or net diffusion current models, the authors suggest that the current generated here is due to the osmotic pressure drop at the inner interface of the tube from the difference in salt concentration. This osmotic pressure drop DP (DP is up to 50 bar for concentration gradient DC = 1 M) that exists inside the double layer is much larger than most external pressure differences (several bar) that can usually be applied. Furthermore, a state-of-the-art 1D NRED device was reported by Feng and coworkers,40 in which work they speculated a single-layer MoS2 membrane with a homogeneous pore size of 10 nm and a porosity of 30% could enable to realize a high power density up to 106 W/m2 in a KCl salt gradient by exploiting parallelization.

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Figure 2. Ion Passive Transport for Salinity Gradient Energy Conversion (A) 1D nanofluidic-based system, 4,000 W/m 2 from Siria et al. 23 (B) 2D layered membrane-based system, 4.1 W/m 2 from Zhang et al. 61 (C) 3D porous membrane-based system, 5.1 W/m 2 from Zhu et al. 34 (D) The development requirements of NRED system and its influencing factors mainly including nanofluidic (membrane) properties, working solution, and electrode.

From a materials perspective, a 1D carbon nanotube (CNT) has great potential toward salinity gradient energy conversion because of distinctive enhanced water flow across it,41 but it has been less explored.42 In addition, the recently developed other 1D materials, such as BN tubes23 or WS2 tubes,43 also hold great potential to build NRED systems. Despite the high power density of 1D-nanofluidic-based NRED, it is worth noting that most of the authors working on 1D materials use the cross-sectional area of one nanochannel to calculate the power density, which is not realistic in practical applications, as channels all have walls and polarize each other when densely packed.44 It remains to be demonstrated how such results can be really scaled up to larger membranes. This is a crucial condition for real blue-energy conversion. Meanwhile, there are other practical limitations, as the fabrication of 1D nanofluidic devices still relies on expensive scientific equipment and laborious material-processing steps, which currently makes predicted system cost unbearable high. Different from the 1D nanofluidic model cases, which simply offer controllability for both experimental measurements and theoretical analysis, 2D nanofluidic structures

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provide the possibility to enhance both power density and membrane size for practical applications.45–47 2D materials have been widely used as building blocks for separation membranes,48 in which efficient rejection by steric effects occurs, as well as electrochemical capacitors. In this way, the enhancement of ion transport is achieved in slit-shaped 2D nanochannels.49 Therefore, 2D materials may be potential candidate to solve the scaling-up problem of NRED application in a facile and cost-efficient way.50–52 2D-material-based membranes, including graphene,53 carbon nitride,54 vermiculite,55 and MXene,56 can always be constructed via facile and cost-effective vacuum filtration or drying of the solution of exfoliated 2D nanosheets (Figure 2B). The interlayer distance is controllable, even as narrow as 1-nmwide,50,57 which guarantees that transport of ions in those membranes is possible. Graphene oxide membranes (GOMs) were the first 2D material to be demonstrated as an ideal platform for nanofluidic ion transport.58 Afterward, many different graphene-related membranes or graphene-composited membranes were explored to extract energy from salinity gradient.8,59 A typical example of GOMs is reported by Guo and co-authors.53 By coupling one pair of oppositely charged GOMs in a three-compartment electrochemical cell, they realized the output power density of 0.77 W/m2 by mixing 0.5 M NaCl artificial seawater and 0.01 M NaCl river water, as well as a high series voltage up to 2.7 V by tandem GOM-NRED stacks. Actually, the way of construction of composite membranes with an asymmetric structure or the surface charge will be the key question to realize surface charge gradient along the nanopores and thus will create the required condition for diode fluidic response and high energy density.60 Most recently, a MXene/Kevlar nanofiber composite membrane was reported to show high power density up to 4.1 W/m2 when used for harvesting salinity gradient power (from 0.004 M NaCl river water and 0.6 M NaCl seawater).61 The authors attribute this good performance to the increased space charge brought by Kevlar nanofibers. On the contrary, their small testing membrane area of mm2-scale is still far below realistic conditions because power density may be seriously lowered with the area of the membrane. In addition, membrane thickness will obviously affect the energy conversion density and efficiency.3 The power is expected to scale inversely with the membrane thickness. Therefore, how to fabricate thin but mechanically stable 2D membrane with high surface or space charge density will be a key step to realize high selectivity and high ionic flux to boost energy density effectively. The recently developed 2D materials, such as graphene, transition-metal dichalcogenides, or hexagonal BN, have obvious advantages because of their molecular thickness. Furthermore, these materials can now be fabricated at large scales, and nanopores can be generated by ion beams.62,63 From an application point of view, several aspects of 2D-membranebased systems also need to be addressed and improved before moving one step further, such as how to increase porosity to decrease membrane impedance and how to maintain excellent mechanical strength at ultrathin geometry. Considering the scaling-up problems for NRED, 3D porous membranes could become the first realization for constructing a facile, high-efficiency harvester with high output power (Figure 2C). Membrane-based technology is well elaborated for many applications in different areas, including seawater desalination, carbon fixation, gas separation, and the water-energy border, due to low energy requirements, controllable design, ease of implementation, and cost-effectiveness.64 Therefore, 3D porous membranes could be a good platform for salinity gradient power generation, on condition that the membrane should be both highly permeable and highly selective (or rectified), a trade-off in general difficult to trade off.65

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3D porous membranes with high pore density and nanometer pores should be potential candidates.66–68 Yang and coworkers first showed68 that mesoporous silica thin film is suitable for proton transport. Later, another group led by Daiguji69 further demonstrated a mesoporous silica-based nanofluidic energy-harvesting system, in which system a maximum power density of 3.9 W/m2 could be obtained under the concentration gradient 300 mM/0.1 mM KCl solution. As an alternative material, mesoporous carbon has long been produced in large quantities and used as an adsorbent in gaseous or liquid adsorption.70 By fabricating mesoporous carbon/ macroporous alumina composited membrane, Gao and coworkers71 realized a power density of 3.46 W/m2. Following the strategy of asymmetric membrane,60,72 a new system consisting of negatively charged hexasulfonated poly(aryl ether ketone)s and positively charged poly(ether sulfone)s with pyridine pendants was fabricated and realized an output power density of 2.66 W/m2 by mixing seawater and river water, and 5.10 W/m2 at a 500-fold salinity gradient.34 All these works demonstrate that the efficient generation of salinity gradient energy by 3D membranes is indeed possible and promising. In terms of materials metrics, large-scale fabrication of ion-selective polymer membranes is well known, is of comparably low cost and large scale, and is already made on the km2 scale. In addition, the thickness of these highly permeable and selective membranes can be decreased to sub-10 nm by interfacial polymerization,73 which shows the potential to decrease membrane impedance and boost the power density efficiently. Despite the advantages of easy fabrication, high flux and throughput, and mature technology to scale up, the 3D porous membranes still meet a bit of gap to achieve high power density. Considering the limitation to improve the conversion efficiency of these conventional structures, NRED research should be focused to improve the existing nanofluidic materials and to optimize geometrize, to go along with the nanoscale phenomena occurring within the porous structures.3,74 Two most important key questions for the further development of NRED are how to realize high power density and how such high power density can be scaled up to an industrial level (Figure 2D). Firstly, the structure and surface charge properties of the pore system are very important for the ion transport and the power generation.32,33,75 It was said that narrow pore diameter and high surface charge density are beneficial, while high permeability (high ionic current density) can benefit from a thin membrane, short fluidic channels, or large channel diameters.76 Meanwhile, theory has predicted that the asymmetric membrane structure with ion rectification can block the ionic backflow thanks to the diode character, in this way boosting the output power by reducing joule loss.77,78 On the other hand, there is no doubt that the power density can be improved by combining different working solutions,39,79 such as solution pairings with higher salinity gradient, integrating salinity gradient with pH gradient or with a temperature gradient. Li et al.80 demonstrated a cellulose ionic conductor that can additionally harvest low-grade heat energy, which provided a possibility to enhance energy conversion efficiency by integrating heat gradient and salinity gradient. Despite the corresponding low efficiency, the source of higher salinity gradient is a problem because the salinity gradient energy between seawater and river water is the largest easily available potential. Electrode and cell layout or engineering will also affect the power density of NRED. Because of the gap between ions and electrons in the NRED process, Ag-AgCl electrodes as a transducer are widely used now. However, this consumable electrode is only suitable for the laboratory research, while industrial application relies on fuel-cell like geometries and layouts. Therefore,

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new thin electrodes, e.g., noble porous carbons81 should be introduced to NRED system. They have to be lightweight, porous, and electrochemically stable but effective to close the salinity gradient energy-to-electricity conversion cycle or act as an ionic supercapacitor to store salinity gradient energy directly.82,83 Last but not least, it should be noticed that most of the reported NRED systems with high power density23,34,40,61,84,85 only test performance on a limited membrane area low to micrometer scale and did not compare the power density with other commercial ion-exchange membranes under the same conditions. As an exception, Gao et al.71 demonstrated that their NRED system has a better power density but lower energy conversion efficiency than commercially available cation exchange membranes. With the theoretical understanding of NRED,86,87 more attention should be reserved for assessing the reliability of the processes by testing large membrane area and referencing performance in a certified fashion under standard conditions, as it is done with solar cells. The potential of salinity gradient energy extraction using NRED has been discussed from 1D nanofluidic structures to 3D porous membranes. Comparing their power densities, it can be clearly observed that the power density of 2D nanofluidic-based NRED and 3D porous-membrane-based NRED is generally lower than 1D nanofluidic-based NRED, which is due to mutual polarization and other interactions between the single channel also throughout the membrane materials.88,89 The recent power density for large-scale 2D/3D membrane-based NRED seems close to the requirement for industrial application, while scale-up problems should be solved before moving one step further because the power density decays drastically when increasing test membrane area. Meanwhile, it is also necessary to scale up to increase potential and current. For example, Schroeder and coworkers90 reported a cation- and anion-selective hydrogel system, which can generate total open-circuit potential differences in excess of 100 V by a scalable stacking or folding geometry. Beyond that, further research is also needed to improve anti-fouling and mechanical performance of membranes. Ion Active Transport for Solar Energy Conversion In nature, solar energy can be harvested and stored mainly by two methods. One is found in the photosynthesis of green plants.91 The other method is simpler and used by some archaea, such as Halobacterium halobium.92 Photosynthesis works via photo-induced charge separation, while archaea uses photo-isomerization, but both of them use these changes to pump protons from low concentration to high concentration to create an electrochemical potential. This ion gradient then drives a molecular machine to produce ATP, i.e., the light energy is converted into osmotic energy, which then is transduced into the chemical energy molecule. Either way, electrochemical gradients are formed after light-induced ion pumping process and are utilized to power various biological processes. In brief, active ion transport against a concentration gradient across a cell wall, which is operated by ion pump, is the key point for this ‘‘ionic’’ mode of solar energy harvesting and storage. To mimic nature, artificial light-driven ion pump for ion (proton) active transport is therefore the first step. In recent years, the construction of artificial ion pumps converting light energy to electrochemical gradients and electrical energy have been realized mainly by light-induced charge separation,93–95 photo-isomerization,96,97 and solid-state nanochannels.98,99 Light absorption and light-induced charge separation are the primary and ubiquitous steps in all photo-energy processes.91,100 In photoproteins of green plants,

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Figure 3. Illustration of Energy Utilization in Energy Conversion by Artificial Ion Pumps (A) Model 1: Proton pump based on artificial photosynthesis center. Adapted from Steinberg-Yfrach et al. 101 (B) Model 2: photo-isomerization induced ions pump. Sp, spiropyrans; Mc, merocyanine; McH +, protonated merocyanine. Adapted from Xie et al. 96 (C) Model 3: Ion pump based on solid-state nanopore. Adapted from Xiao et al. 108

numerous chromophores are used to achieve the separation of charges and to avoid back reactions. To realize the photo-induced electron transport process in vitro, a complex and multifunctional artificial reaction center was used to transfer charge to electron donors and acceptors in solution, with the donors and acceptors being spatially separated. These transfers have to occur faster than the charge recombination or lifetime of the excited state. Moore et al.101 reported a molecular triad Q–P–C containing carotenoid (C), porphyrin (P) and naphthoquinone (Q) moieties for light-induced proton pump. (Figure 3A, upper draw.) The artificial proton pump can be fabricated by doping Q–P–C and a proton shuttle (Qs: 2,5-diphenylbenzoquinone) to a liposomal bilayer membrane. The proton translocation across the bilayer membrane involved seven steps (Figure 3A, down draw). The first excitation step included two intermediate states, in which the triad undergoes two-step charge separation. The first intermediate was Q –P+–C, resulting from the photo-induced electrons transfer with a quantum yield of 1. The second intermediate Q –P–C+ was generated by electron transfer from the carotenoid to the porphyrin radical cation with quantum yield 0.15. In step 2, Q –P–C+ was formed by passing electron to Qs near the external aqueous medium. In step 3, a proton from the external aqueous medium combined with Qs to form QsH. In step 4, QsH diffused across the bilayer membrane. In step 5, the QsH was oxidized by the radical cation of Q–P–C+ to form Qs+H and Q–P–C. In step 6, the proton was released to the internal aqueous medium. In step 7, the Qs diffused to the external aqueous again. The sum of steps 1–7 describes the conversion of photo energy to chemical energy. Analogously, other artificial photosynthesis centers94,102 also have been synthesized and even used to pump Ca2+ ions.103 Taking a different way, bacteriorhodopsin existing in some archaea can pump protons transport by photo-isomerization.104 Generally speaking, a retinal molecule in the bacteriorhodopsin can absorb light energy and experience photo-isomerization and then rearrange the proton conductive pathway and pump the proton across the liposome membrane. Therefore, this simple light-energy-harvesting system

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through photo-isomerizing molecules can provide a concept for synthetic systems. In fact, many different photochromic compounds also experience changes in the molecular configuration after light absorption and then can be designed to realize artificial pump functions.105 The artificial photo-isomerization ion pump can be simplified as Figure 3B, upper draw. The photo-controlled molecular switches are incorporated into membranes, which are used for separating two chambers containing the ions. The pump process can be realized directly by a change of molecular configuration, resulting in a net charge separation and an electrochemical gradient. Bakker and coworkers96 reported an artificial proton pump for photoelectric energy conversion by embedding spiropyran into polymeric liquid membrane (Figure 3B, down draw). In step 1, the ultraviolet light induced a ring-opening reaction converting spiropyran (Sp) to merocyanine (Mc). In step 2, the merocyanine combined with H+ diffused across the membrane driven by concentration gradient. In step 3, protons were released on the other side when the membrane is irradiated with ultraviolet and visible light. In this way, a proton concentration gradient can be generated, and photoelectric energy conversion can be realized based on the diffusion of protonated merocyanine (McH+). Beyond that, some simpler solid-state nanopore-based artificial ion pumps were also realized.98,106,107 The first photo-driven artificial ions pump was reported based on a single polyethylene terephthalate conical solid-state nanochannel.99 However, in this system, the photo-induced surface charge changing can only drive ions against a 1.1-fold concentration gradient and is far away from creating an effective gradient for the chemical potential generation. Recently, a carbon nitride nanotube membrane-based artificial pump was reported,108 which has enough ‘‘power’’ to pump ions against steep concentration gradient up to 5,000 folds by light irradiation, and can be used for photoelectric energy conversion. The working principle of the ion pump is based on the charge separation of an organic semiconductor, carbon nitride, resulting in the change of surface charge distribution on the inner surface of nanotubes (Figure 3C, upper draw). The photo-induced electric field will drive ion transport against even steep concentration gradients, in which process ionic current and voltage can be generated (Figure 3C, down draw). Another advantage for this solid-state nanochannel based ion pump is that the devices can be easily connected in series or parallel to multiply its limited ionic current or voltage. Similar ion active transport also can be realized by other optoelectronic semiconductors, for example, GOMs.109 All these existing examples are just the first step toward practically employable photo-driven ion pumps and solar energy harvesting. Different approaches and appropriate materials are needed to support feasible mechanism before artificial ion pumps become attractive for solar energy conversion and storage. Three different preliminary approaches to realize artificial ion pumps can be identified. The first one is denoted as ‘‘pseudo ion pump’’ (Figure 4A), as the photo-process does not pump ions from low concentration to high concentration but rather generates an ion concentration gradient by chemical reactions with the aid of photo-responsive molecules in electrolyte110 or photocatalytic reactions.111 The photo-responsive molecules release protons or ions by light irradiation, as such generating a transmembrane proton or ion concentration gradient. With a suitable ion-selectivity membrane, an ion-transport-based pump system that transfers the chemical energy into an electric current can be constructed.

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Figure 4. The Diverse Layouts of Photo-Driven Artificial Ion Pumps (A) Pseudo ion pump. This corresponds to a photo-induced concentration gradient without a pumping process. (B) Chemical ion pump. The ions or protons are pumped mainly based on chemical reactions, e.g., photo-induced insertion reaction. (C) Physical ion pump. The ions or protons are pumped across membrane from a low to high concentration directly without chemical reaction; the solar energy is converted into a concentration gradient.

The second principle is the ‘‘chemical ion pump,’’ which is based on ion transport but also a photoreaction in the pump process (Figure 4B). For example, the photo-insertion reaction has been used to pump protons.112–114 The proton is here first reduced to a neutral species by photo-generated electrons, and the neutral hydrogen-carrier is transported by diffusion. On the other side of the membrane, the protons are released into the electrolyte by using the photo-generated leftover hole to oxidize the transporter molecule again to the proton. This artificial photo-driven ion pump is similar to the proton/electron transfer process in photosynthesis. The third one is best described as a ‘‘physical ions pump,’’ as there are no chemical reactions in the pumping process (Figure 4C). The photo-driven ions transport form low to high concentration can be realized by a photo-responsive membrane, for example, a porous membrane fabricated from semiconductor materials or a polymer membrane modified with photo-responsive molecules where the excited state is charged. The light irradiation will change the surface charge of the membrane99,115 or drive a charge gradient of photo-responsive molecules.96,116,117 These artificial photo-driven ion pumps are similar to the natural ion pumps in bacteriorhodopsin. A common factor for these three different pumps is to build ‘‘an asymmetric configuration’’ by light irradiation, either based on an asymmetric proton, ion, or molecule distribution on both sides of the membrane or asymmetric surface charge distribution of the membrane. For ‘‘pseudo ion pump,’’ ions themselves move uphill driven by a gradient of chemical potential. In this model, photo-responsive molecule is the key, while the choice of it is limited. For the ‘‘chemical ion pump’’ model, ions are transmitted by mediators. In fact, this model is an upgrade of the ‘‘pseudo ion pump’’ and depends on photo-responsive molecules too.118 For these two models, photo-responsive membranes or photo-responsive molecular modified membranes should be developed in a competitive manner to create a diversity of possibilities for artificial ion pump. For the ‘‘physical ion pump’’ model, ions move to balance the asymmetric surface charge distribution induced by light irradiation. This model

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Figure 5. Two Predictable Integrative Ion Transport Examples (A) Light-driven ‘‘nanofactories’’ can be used for energy generating by the following energy conversion route: light energy/chemical energy/electrical energy. (B) Light-driven ‘‘nanorobot’’ with the bacteria as the model prototype. The nanorobot can move by the following energy conversion route: light energy/ chemical energy/mechanical energy.

should be the most promising ion pump because it works by separation of electrons and holes induced by light. In terms of this view, all the photo-responsive organic and inorganic semiconductor materials or their heterojunction derivatives can be used to build photo-driven ‘‘physical ion pump.’’ There is no doubt that their (heterogeneous) nanostructure is the key factor for the further development of photo-driven artificial ion pumps for energy harvesting, as crucial factors are ion mobility, selectivity, and separation of cations and anions, as well as a most effective conversion of light into electric field gradients by material and structure. In addition, the electrode is another key factor when light energy has to be converted in final electric energy, similar with NRED system discussed above. Conclusions and Perspectives For moving to visions, we of course have to mention that nature is not really interested in electricity, and molecular machines such as ATP-synthase or the (related) rotational motor of a flagellum directly transfer chemical potential difference into energy storage molecules (ATP) or mechanical propulsion. Figure 5 sketches two artificial (and hypothetical) nanomachines, which, by incorporation of active and passive ion transport subunits, turn into integrated ‘‘nanofactories’’ for energy conversion or ‘‘nanorobot’’ for further application. The ‘‘nanofactory’’ or ionic photovoltaic cell (Figure 5A) is an integrated energy generator driven by ions pump, which can pump ions from low concentration cell to high concentration cell and store light energy into osmotic energy by special ion-selective membrane, like nature. Then, the osmosis unit or NRED system can convert the chemical potential energy to electrical energy. By serial connection, energy production efficiency and open-circuit potential can be scaled up. In fact, it is a commendable approach to improve low energy density of these ion-transportbased energy-harvesting systems, which also has been practiced for other similar systems, such as integration of low-grade heat energy and salinity gradient energy.119 A recent work by Radenovic and coworkers120 also shared a different

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but similar idea to ‘‘nanofactories.’’ In their work, the osmosis energy generated by single MoS2 nanopore can be further enhanced by light irradiation because light increases the surface charge of atomically thin MoS2 membrane, followed by an increase of the ion selectivity and the surface conductance of MoS2 nanopore. To move one step further for practical application, we believe a closed loop system with integrated ion active/passive functions will be more efficient as an energy generator with advantages of low cost, low pollution, and safety. The light-driven ‘‘nanorobot,’’ which is to be developed with the bacteria as the master pattern, is another example of an envisioned artificial nanomachine driven by ion transport (Figure 5B). In the head part of ‘‘nanorobot,’’ a light-driven artificial ion pump is used to pump ions from low concentration to high concentration to build up concentration difference for chemical potential. In the stern part of ‘‘nanorobot,’’ the chemical gradient can be converted into mechanical energy by driving a biological, integrated flagellum motor.74,121 Such task-delivering machine subunits are the first step to more complex, autogenous ‘‘machine-system integration.’’ Nature has taken a billion years to develop two as such optimized approaches to harvest solar energy as intermediary osmotic energy: as a part of the energy chain in photosynthesis of green plants and photo protein based gradients in some archaea.92,122 However, we also should never forget that chemical potential energy is rather ‘‘diluted,’’ i.e., even the best synthetic pump can only store ca 0.2 MJ/kg, this is ca. 10 % of a Li-ion battery or around 1 % of chemical energy storage in molecules but comparable of storing sun energy in hot water. Similar dilution rules hold true for energy generation from salinity gradients, and large volumes must be manipulated to come up with reasonable amounts of energy. There is still a gap for its large-scale exploitation because of the lower efficiency of current conversion schemes, but there are new scientific tools and approaches to improve that. For us, a potential roadmap for material scientists is rather clear: both green plant photosynthesis and bacteriorhodopsin, as well as an electric eel, can handle the dilute character of the energy, and we can expect that an alternative ion/proton transport based photovoltaic systems can reach at least the same energy conversion efficiency as an electron based photovoltaic system. On top of these arguments, ‘‘salinity gradient energy’’ seems to be further developed than active ion transport from solar energy and has reached a technology readiness level very close to practicality.3 There is no doubt that the combination of such an ion passive membrane with ion pump membrane of similar flux performance would, of course, enable higher efficiency integrated devices. We expect that ion-transport-based systems including passive transport and active transport could turn into a new paradigm for clean energy harvesting and hope that ion-transport-based photovoltaic systems can move one step further, e.g., via simultaneous ATP synthesis within the nanocompartments or other nanomachining approaches. Even novel, currently unseen ion-transport-based energy-harvesting system could show up, as the game just started.

ACKNOWLEDGMENTS K.X. acknowledges the support of the Alexander Von Humboldt Foundation. This work was financially supported by Max Planck Society and National Key Research.

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AUTHOR CONTRIBUTIONS K.X. and L.J. initiated this review; K.X. and M.A. wrote the manuscript; L.J. assisted in the literature review and provided input for discussions.

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