Desalination 458 (2019) 97–115

Contents lists available at ScienceDirect

Desalination
journal homepage: www.elsevier.com/locate/desal

Engineering advance

Biomimetic membranes as potential tools for water purification: Preceding T

and future avenues
⁎ ⁎
Ahmed Fuwada,b, Hyunil Ryub,c, Noah Malmstadtd, Sun Min Kima,b, , Tae-Joon Jeonb,c,
a
Department of Mechanical Engineering, Inha University, Incheon 22212, Republic of Korea
b
Biohybrid Systems Research Center (BSRC), Inha University, Incheon 22212, Republic of Korea
c
Department of Biological Engineering, Inha University, Incheon 22212, Republic of Korea
d
Mork Family Department of Chemical Engineering and Materials Science, University of Southern California, Los Angeles, CA 90089, USA

A R T I C LE I N FO A B S T R A C T

Keywords: Industrialization and urbanization lead to increased generation of wastewater causing serious environmental
Aquaporin biomimetic membranes pollution and deterioration of water quality. Membrane-based water treatment represents a major technological
Reverse osmosis approach to addressing global water scarcity and environmental pollution issues. However, there has been re-
Forward osmosis latively little progress in membrane technologies for water treatment mainly due to the inherent limitations of
Electrodialysis
membrane materials and membrane fabrication techniques. In recent years, biomimetic membranes, such as the
Membrane distillation
Water desalination
aquaporin membrane, have emerged as strong candidates for membrane-based water purification technology.
Biomimetic approaches have the potential to overcome the problems associated with existing membranes in-
cluding limited permeability, low selectivity, and excessive energy consumption. But industrial-scale defect-free
biomimetic membrane fabrication remains a major challenge. Key factors that must be addressed to overcome
this challenge include protein stability, membrane housing materials, and the surface chemistry and structural
characteristics of the substrate. This paper reviews the state-of-the-art of membrane-based water purification
technologies, summarizing the role and limitations of conventional membrane materials while evaluating the
latest progress in the field of biomimetic membrane fabrication. We conclude that a thorough understanding of
the relationship between substrate structure-surface properties and membrane performance is necessary for the
further development and commercialization of aquaporin biomimetic membranes.

1. Introduction
According to the UN Water Development report, one out of six
people today have insufficient access to safe freshwater [1]. Rapid
population growth, industrialization, and increasing global warming
are the major factors exasperating global water scarcity. The continuous
release of complex waste effluents from manufacturing industries,
agricultural production facilities, and municipalities causes serious
contamination to freshwater resources like lakes, rivers and oceans.
Therefore, developing new methods for recovering fresh water from
municipal and industrial wastewaters is a key research area [2]. To take
advantage of the full potential of these emerging sources of fresh water,
novel separation and purification technologies are needed [3,4].
Membrane-based water treatment technologies produce high-
quality water with less energy consumption compared to other con-
ventional water treatment technologies [5]. Currently, several mem-
brane separation techniques like reverse osmosis (RO), forward osmosis
(FO), membrane distillation (MD) and electrodialysis (ED) are available
for water desalination. Among them RO is the most widely utilized
membrane separation technique for water desalination and almost over
55% of desalination plants in the world are based on RO [6,7]. Fig. 1.
shows the commercial desalination technologies with operating prin-
ciples.
Membranes for water purification are usually made from polymeric
materials. Existing membrane fabrication technologies lack molecular
scale design which limits the performance of the membrane selective
layer [8,9]. There has been little improvement in membrane perfor-
mance with incremental improvements in polymeric membrane mate-
rials. However, recent advancements in bio- and nanotechnology have
emerged as alternative approaches to overcome the shortcomings of
conventional membranes. These developments have led the material
sciences toward the revolutionary field of biomimicry, in which re-
searchers imitate natural phenomena to solve complex science and
engineering problems [10,11]. Biomimetic membranes are products of

⁎
Corresponding authors.
E-mail addresses: sunmk@inha.ac.kr (S.M. Kim), tjjeon@inha.ac.kr (T.-J. Jeon).

https://doi.org/10.1016/j.desal.2019.02.003
Received 7 June 2018; Received in revised form 16 January 2019; Accepted 8 February 2019
Available online 22 February 2019
0011-9164/ © 2019 Elsevier B.V. All rights reserved.
A. Fuwad, et al.
Fig. 1. Illustration of different desalination technologies. Non-membrane based technologies (distillation) works on the thermal evaporation, in membrane based
technologies the driving force can be pressure (osmosis), temperature, or salinity gradient across the membrane. For FO, water diffuses to high salinity side, in RO,
water diffuse to low salinity side because of hydraulic pressure. Whereas in ED &MD, the driving force is salinity and temperature gradient respectively. Aquaporin
Biomimetic membranes are the potential replacement of conventional FO and RO membranes and fabricated in two structural design, planar bilayer or vesicle
embedded.
such research.
Of particular interest, aquaporin, a major intrinsic protein (MIP),
allows the passage of water across cell membranes in biological systems
[12]. Aquaporin is also known as a water channel that has high se-
lectivity and permeability for water molecules but prevents the passage
of ions and other impurities completely. The application of aquaporin
for use in water treatment has gained great attention in the water
treatment industry [13–15]. The selectivity and permeability of aqua-
porins are nearly incomparable to those of any man-made membranes
and their corresponding technology. To date, many attempts have been
made to develop methods for the construction of biomimetic aquaporin
membrane systems for water purification, including vesicle fusion
[16,17], vesicle adsorption [18], chemical crosslinking [19], interfacial
polymerization [20] and magnetic-aided adsorption [21].
In this review we summarize the latest progress and development in
aquaporin biomimetic membranes based on the surface conjugation
methods and substrate materials. Our review not only provides a the-
matic description of the methods used to construct biomimetic aqua-
porin membranes on solid substrates but also explains their effects on
membrane performance. A brief comparison with conventional mem-
branes is also presented. This work also places emphasis on the basic
principles of conventional technologies, with a discussion of their ad-
vantages and disadvantages to highlight their current limitations.
Finally, topics regarding the commercialization of aquaporin mem-
branes and their optimistic future are discussed.
2. Conventional membrane-based technologies
The successful implementation of membrane-based technologies
depends upon membrane materials, which can be divided into two
categories: (i) organic and (ii) inorganic. Organic membranes have
dominated the membrane-based water purification industry mainly
because of their tunability, improved performance and low cost.
Membrane technologies are often categorized based on their driving
force, which may be pressure, electricity or temperature. Reverse os-
mosis (RO) is a pressure-driven process and requires special membranes
98
Desalination 458 (2019) 97–115
to withstand high-pressure and high-temperature conditions. Forward
osmosis (FO) uses natural osmosis for water purification and possesses
several advantages, such as low energy consumption, long membrane
lifespan and low fouling because of the absence of pressure, but FO still
exhibits suboptimal water flux and recovery. Draw solution develop-
ment and specialized membrane materials are the weak areas of FO. To
overcome the disadvantages of the above processes, hybrid processes
have been developed. Electrodialysis (ED) is one such process; it uses
electric current to separate ions from the feed solution. For low salt
concentrations, RO becomes uneconomical, but ED exhibits excellent
performance. Another hybrid membrane-based water-sweetening
technology is membrane distillation (MD). Water sweetening is ac-
complished by the partial vapor pressure difference caused by a tem-
perature gradient across a hydrophobic porous membrane. The hydro-
phobic membrane allows water vapor to pass through instead of liquid.
MD has several advantages over other technologies, the most important
of which is the low operational cost; additionally, the product quality is
independent of the salt concentration in the feed solution, as in RO and
ED. These processes are summarized in detail with their energy con-
sumption, advantages and shortcomings in Table 1. The next section
provides more details of the above technologies including their com-
mercial presence, membrane materials and limitations.
2.1. Reverse osmosis
2.1.1. Overview
In RO, water moves across a semipermeable membrane against os-
motic pressure. There is increasing interest in this technology due to the
development of novel membrane materials, energy recovery methods,
and feed pretreatments [22].
2.1.2. Current technology
RO systems generally employ cross filtration, where the feed passes
through the filter media in two directions. The filtered water goes one
way while the contaminants go another, allowing the water to sweep
any contaminate buildup. RO systems can easily remove 95 to 99% of
A. Fuwad, et al. Desalination 458 (2019) 97–115

dissolved salts, solid particles, biological contaminants and other or-

[33,191,192]
References

[188–190]

[194–196]

[120,121]
ganic contaminants from the feed [23]. The rejection efficiency relies

[56,193]
upon two factors, i.e., the charge and size of the molecule. The removal
capability increases as these factors increase. However, RO systems
cannot remove gases, such as CO2, due to no ionization in the solution.
High operating and capital cost, fouling, low

Low transmembrane flux, membrane fouling,

High cost, short membrane life, membrane

operations, difficult to scale up technology

An RO plant consists of four major units, the pretreatment, pumping,

Fragile, cannot withstand high-pressure

Solute leakage, internal improper draw
membrane assembly and post treatment units. Before a feed is sent

Study shows that reduced transmembrane resistance can decrease energy cost by 88% and saves around $1.145 million/yr for desalination plant of capacity 100 million liter per day [197].
directly to the RO membrane assembly, it is pretreated to remove un-
permeability, short membrane life

wanted elements, such as suspended particles, biological contaminants

solution (flux enhancement)

and macromolecules, to prevent potential damage to the membrane

for industrial applications

assembly. In addition to dechlorination and pH treatment [24], micro-
high temperature and ultrafiltration are performed to remove suspended and biological
contaminants [25,26]. The pretreated feed solution is then pressurized
and sent to the membrane assembly unit for further purification. A
Limitations

semipermeable membrane allows the passage of water through it while

fouling

retaining the salts [27,28].

2.1.3. Membrane materials

nonvolatile solutes, low operating
cleaning cost and long membrane
Ultrapure water, high mechanical

As RO works against osmosis, a large amount of pressure is needed.

Low energy consumption, lower

fouling, high salt rejection and

Complete removal of dissolved
Ionic solutes, ultrapure water

A variety of polymer-based membranes that can withstand this high

Low energy consumption, no

pressure are employed, and they can be broadly categorized as cellulose

acetate (CA) or non-CA (e.g., polyamide and polysulfone [Psf]), as
shown in Table 2. Noncellulose polyamide is the most commonly used
life, low fouling

material for RO membranes because of its high water permeability and

Advantages

salt rejection. These membranes consist of a porous support with an

water flux
pressure
strength

active thin polyamide layer; this active layer is responsible for salt re-
jection and water permeability. Additionally, these membranes offer a
wide range of operational pH (4–11) and temperature ranges but are
highly sensitive to oxidizing agents. The major drawback of polyamide
PE, PVDF with charged

membranes is fouling, which is mainly related to the hydrophobicity of

Polymeric membrane

ionic groups (NH3+,

materials (TFC, CA)

membrane surface. Many studies have reported improvements in active

Commercial base

layer fouling resistance using surface modifications. CA is another

PTFE, PP, PE

choice for RO membranes. The very first type of water purification

materials

CA, TFC

COO−)

membrane was fabricated using cellulose diacetate (CDA), and this

Psf

membrane showed 98% salt rejection but poor water permeation [29].
Cellulose triacetate (CTA) membranes were subsequently synthesized
and showed improved chemical and mechanical stability and enhanced
purification, compound recovery
Concentration of solution, water
(desalination and production of
Microsolute and salt separation

chlorine resistance. The properties of these membranes can be en-

Ion filtration, organic solvent
Desalting of ionic solutions,

hanced by blending the CTA with other polymers or monomers; these

concentration of solutions
Water purification, power

membranes show high resistance to chlorine and oxidizing agents but

have a very narrow operational pH range (4–6) due to hydrolysis. Their
ultrapure water)

nonpolar and smooth surface makes these membranes more resistant to

fouling but at the expense of low salt rejection and water flux.
Applications

generation
Summarization of commercial membrane-based desalination technologies.

filtration

2.1.4. Challenges
Despite the several advantages of RO, including ultrapure water
filtration, high permeate flux and salt rejection, its performance is
2.3–12.5 kWh/m3

1.0–3.0 kWh/m3

0.5–1.3 kWh/m3

compromised in terms of product quality and energy consumption

consumption

when the salt concentration in the feed is low [30]. The most important
0.5–5 bar

challenge is fouling; new membrane materials are needed to overcome

Energy

n.a.a

this critical problem. Moreover, membranes used in RO are more prone

to fouling and mechanical damage than those used in other methods
Concentration gradient

because high pressure continuously pushes particles into the mem-

concentration gradient
Temperature gradient

brane, which ultimately blocks the membrane. These particles become

Pressure gradient

Electric potential
Driving force

Table 2
Pressure/
gradient

Various types of polymeric membranes used in RO desalination. These are ca-

tegorized as cellulose and non-cellulose based material.
Cellulose Non-cellulose
Separation process

Cellulose diacetate Polyamide (aliphatic or aromatics)

Forward osmosis
Reverse osmosis

distillation

membrane

Cellulose triacetate Polyurea

Electrodialysis

Polysulfone
Biomimetic
Membrane

Sulfonated polysulfone
Table 1

Polyvinyl alcohol derivatives

Polypiperazides
a

99
A. Fuwad, et al.
Table 3
Comparison of FO and RO membranes at a commercial site [36,37].
Parameters RO membrane assembly FO membrane assembly
Feed recovery (%) 25 35
Water flux (m3/h) 3.0 4.2
Feed pressure (bar) 65 4 Low biofouling
Pumping power (85% eff.) 25.3 kW 1.6 kW
lodged inside the membrane, rendering membrane cleaning very diffi-
cult or almost impossible. Additionally, expensive pretreatment pro-
cesses, high-energy pumping stations and very large membrane areas
increase the cost dramatically [31,32].
2.2. Forward osmosis
2.2.1. Overview
FO is an emerging water purification technology that uses an os-
motic pressure difference to drive water across a semipermeable
membrane. Due to its potential applications in several areas, including
food and drug preparation, desalination and power production, re-
search on FO membranes has increased exponentially [33,34].
2.2.2. Current technology
FO systems have the potential to overcome RO technology because
of their low energy consumption and high fouling resistance. Long-term
operations may cause fouling, but 90% of the water flux can be easily
regained by backwashing without any chemical treatments mainly be-
cause it is surface fouling that occurs [35]. A brief quantitative com-
parison between RO and FO at the plant site is given in Table 3.
2.2.3. Membrane materials
FO membranes are fabricated with a thin selective layer for high
water selectivity and a porous support layer to increase the mechanical
strength of the membrane [38]. However, recent studies have shown
that the thickness and porosity of the support layer leads to internal
concentration polarization (ICP), which reduces the osmotic driving
force [39,40]. In addition, wetting of the support layer plays an im-
portant role in membrane performance. If the membrane is not fully
wet, air or vapor trapped within the membrane not only blocks the
pores but also increases the ICP, reducing its effective porosity and
consequently the water flow [41]. CA membranes are less susceptible to
bio- and thermal degradation due to their high chlorine resistance [42].
However, low water permeability and a narrow operational pH range
limit their commercial presence [43]. Recently, HTI© developed a new
thin-film composite (TFC) FO membrane that exhibits better perme-
ability, salt rejection and high pH tolerance, with an operational range
of 2–12 [44]. The TFC membrane comprises a thin selective layer
supported by a porous thin support layer, while the mechanical strength
is provided by polyester mesh. The selective layer was made more
hydrophilic than a CA membrane to avoid membrane biofouling [41].
To date, several studies have reported methods to overcome the fouling
and low permeability of FO membranes by surface modifications
[45,46], the blending in of different polymers and the incorporation of
nanoparticles in the active layer [47].
2.2.4. Challenges
FO still faces some challenges in critical areas, such as draw solute
recovery [48–50], concentration polarization [51] and reverse solute
diffusion [52]. Table 4 lists the advantages and disadvantages of FO,
which are intertwined with each other. For instance, draw solute can
affect the concentration polarization by its viscosity, ionic size and
diffusion coefficient [51]. Similarly, membrane materials with low
porosity and selectivity can increase reverse solute diffusion, which in
turn can increase membrane fouling [53]. Studies are being performed
100
Desalination 458 (2019) 97–115
Table 4
Illustration of FO process advantages and limitations.
Advantages Limitations
Low energy requirements Draw solution recovery
High membrane lifespan Reverse solution diffusion
Concentration polarization
Processing high suspended solid feed
to improve current and identify novel materials for FO systems with
high selectivity and porosity. Moreover, water recovery from draw so-
lution is a major challenge and limits FO applications. Several research
groups are focusing on developing energy-efficient draw solution re-
covery systems [54].
2.3. Electrodialysis
2.3.1. Overview
ED utilizes electric current to separate ions from water [55,56]. ED
consists of different cell compartments separated by selective ion ex-
change membranes; under applied direct current, the ions move toward
the electrodes by passing through these permselective membranes [57].
The whole process is carried out in a confined cell, called an ED cell,
with the following main parts: (1) an ion exchange membrane semi-
permeable to ions; (2) electrodes that provide the force to separate the
ions/solute [58]; and (3) electrolytes that fill space between the elec-
trodes to allow the follow of current.
2.3.2. Current technology
When a potential difference is applied across the electrodes, cations
tend to move toward the cathode by passing through a cation-exchange
membrane (CEM), which allows the passage of cations while retaining
anions and uncharged species; anions are directed toward the anode
and diffuse through the anion exchange membrane (AEM), which al-
lows only anions to pass while rejecting cations [59]. The performance
of ED depends upon different parameters, such as the feed flow rate
[60], current density [61], membrane permselectivity [62], and feed
and product concentrations [60]. ED is 25% less costly than RO [63],
can selectively remove many ions, including nitrates [64], and has no
effect on uncharged materials, such as silica. The most significant ad-
vantage is its antifouling cycle; fouling can be removed by reversing the
electrode polarity, which is a process known as electrodialysis reversal
(EDR) [65].
2.3.3. Membrane materials
Ion exchange membranes should have the following properties: (1)
high permselectivity; the membrane should be highly permeable to
counterions and impermeable to co-ions; (2) low electrical resistance;
under a driving force, the membrane permeability should be as high as
possible; (3) mechanical stability; the membrane should not swell or
shrink during the change in solution concentration from concentrated
to dilute; and (4) chemical stability; the membrane should be able to
withstand varying temperatures and pH levels, as well as oxidizing
agents [66,67]. Ion exchange membranes mostly consist of inorganic
materials containing either a fixed cationic group (e.g., NH3+, NRH2+,
NR2H+, and NR3+) that prevents the passage of cations, i.e., AEMs, or a
fixed anionic group (e.g., SO3−, COO−, PO32−, and PO3H−) that per-
mits the passage of cations, i.e., CEMs. Ion exchange membranes are
usually categorized into two main types: (1) homogenous, with che-
mically bonded charged groups; and (2) heterogeneous, with charged
groups physically mixed with the membrane matrix [68]. Organic
membranes consist of a mixture of different polymers (e.g., PE, PP, and
PVDF) [69–71] and block copolymers (BCPs) [72] containing ionic
groups, such as acrylic, methacrylic [73,74], and acrylonitrile [75].
Inorganic membranes can also be fabricated from zeolites and
A. Fuwad, et al. Desalination 458 (2019) 97–115

phosphate salts, but these membranes are very expensive and have poor ensuring enhanced vapor transport and consequently the overall per-
electrochemical properties. Furthermore, new materials are also being formance of MD. Polytetrafluoroethylene (PTFE), polyvinylidene
adopted, such as organic-inorganic hybrid membranes [76] that exhibit fluoride (PVDF), polypropylene (PP) and polyethylene (PE) are highly
high flexibility and mechanical, thermal and chemical resistance. hydrophobic and thermally stable and are commonly used in MD ap-
plications. The melting point of PVDF is 170 °C, that of PP ranges from
2.3.4. Challenges 130 to 170 °C, while the melting point of PTFE is 327 °C [103]. Recent
Challenges faced by ED include membrane cost, scaling, and short studies indicate that MD performance was improved with the use of
lifespan, as well as unexpected reactions associated with the electrodes PTFE membranes compared to MD with membranes consisting of other
[77]. Some other inherent issues are that ED removes only charged materials because of the non-wettability and high mass transfer coef-
particles and has no effect on uncharged species. Finally, its energy ficient of the PTFE membranes [104]. On the other hand, inorganic
consumption increases with the amount of salt in the feed, and the materials have several advantages in terms of precise pore structure,
process becomes nearly unfeasible when the salt concentration in- mechanical strength and thermal stability. However, such materials
creases to > 3 g/L, which is much less than the salinity of sea water have not yet found any commercial use, primarily because of their high
(35 g/L) [78]. cost and wettability. Inorganic membranes tend to be hydrophilic due
to the presence of surface hydroxyl groups leading to membrane
2.4. Membrane distillation wettability, which makes these membranes unsuitable for MD opera-
tions [105]. A number of surface functionalization methodologies to
2.4.1. Overview fabricate hydrophobic inorganic membranes have been presented
MD is a thermally driven membrane separation process. Separation [106,107]; alumina [108,109], zirconia [110] and silica [111] are the
occurs due to a vapor pressure gradient across a microporous hydro- dominant materials utilized to fabricate such membranes.
phobic membrane. The hydrophobic membrane allows only vapor to
pass through it. MD can be divided into four major configurations based
2.4.4. Challenges
on the vapor collection method. Direct contact membrane distillation
MD technology has been expanded from seawater desalination to
(DCMD) has a simple configuration but causes heat loss due to con-
other areas, such as the recovery of compounds [112], the concentra-
duction. However, it is widely used in the food industry for con-
tion of liquids and the treatment of wastewater [112]. However, this
centrating solutions [79–83] and acids [84–86]. Vacuum membrane
technology still faces many problems related to the cost of membranes
distillation (VMD) applies a vacuum to the permeate side. The major
and the wetting of membrane pores, which causes fouling and scaling
advantage of VMD is that there is no heat loss, but vacuum pumps and
and decreases the flux and lifespan of the membrane [113,114]. Simi-
an external condenser are required. VMD is mainly used for the se-
larly, an increase in membrane thickness decreases permeate flux [115]
paration of volatile components [87–89] and water treatment [90–92].
and increases heat efficiency [116]; thus, an optimal design is needed.
Air gap membrane distillation (AGMD) introduces an air gap between
These problems are outlined and illustrated in Fig. 2.
the membrane and permeate solution, which ultimately reduces heat
loss but increases mass transfer resistance. Sweeping gas membrane
distillation (SGMD) establishes a barrier of inert gas between the 3. Biomimetic aquaporin membranes
permeate solution and the membrane, which decreases thermal polar-
ization but increases cost due to extra equipment and complexity [93]. Biomimetic aquaporin membranes have recently gained importance
Recently, hybrid configurations have been designed to achieve high due to their experimentally demonstrated superior performance in
thermal efficiency for economical operations. These include multistage terms of water flux and salt rejection compared to the conventional
multi-effect membrane distillation (MEMD), in which the feed is pre- membranes [117–119]. Although the first aquaporin biomimetic
heated using permeate vapor to recover heat and condense the vapor
[94]. Material gap membrane distillation (MGMD) introduces a poly-
meric sponge or mesh instead of air to enhance vapor flux [95]. Va-
cuum multi-effect membrane distillation (V-MEMD) is similar to MEMD
with additional vacuum enhancement for optimal heat recovery and
economical commercial-scale operations [96,97]. Memsys®, a major
player in the membrane distillation industry, has installed pilot-scale
facilities with a V-MEMD configuration [98]. In addition to the above
technologies, others, such as permeate gap membrane distillation
(PGMD) [99] and hollow fiber multi-effect membrane distillation (H-
MEMD) [100,101], are under development with the aim of achieving
efficient and cost-effective result.

2.4.2. Current technology

As a hybrid technology, membrane distillation has many advantages
over other conventional techniques, including a low operating tem-
perature and pressure, high desalting efficiency and the removal of
organic solvents and ions, such as nitrates [102].

2.4.3. Membrane materials
Membrane selectivity is controlled by tuning different parameters,
including the pore size, electrical polarity and diffusion coefficient.
Unlike other processes, MD membranes are made to selectively retain
liquid water and allow only vapor to pass through them. During op-
eration, water may cause wetting of the membrane. As a result, the
membrane may lose its selectivity. This selectivity is usually achieved
by employing hydrophobic materials to fabricate the membrane,
Fig. 2. Illustration of MD membrane performance based on different factors.
Membrane hydrophobicity and thickness are the deciding characteristics in
fabrication of MD membranes. Increase in thickness and hydrophobicity de-
creases the wettability and increases thermal efficiency which are highly de-
sirable, but on the other end it decrease permeate flux due to increase mass
transfer resistance. High permeability (flux) can be achieved by decreasing
thickness of membranes but it increases wettability and thermal conductivity
(which cause heat loss across membrane).

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A. Fuwad, et al. Desalination 458 (2019) 97–115

Fig. 3. Aquaporin structural model. (a) Aquaporin

structure from an extracellular angle; the dotted red
line shows the 2-fold axis of two halves of a
monomer; the red square indicates the 4-fold axis of
the tetramer. (b) Structural view parallel to the
membrane. (For interpretation of the references to
color in this figure legend, the reader is referred to
the web version of this article.)
Reprinted with permission from Gonen et al.© 2006
Cambridge University Press [139].

Table 5
Summarization of lipid- and polymer-based vesicle properties.
Lipidic membranes (liposomes) Polymeric membranes References
(polymersomes)

Low chemical stability and fluidity Higher stability (because of [198,199]

(due to low molecular weight) high molecular weight)
High cost Tunable and low cost [167,200]
Short membrane lifespan Long membrane life cycle [167,199]
Uncontrolled/high permeability Controlled/low permeability [119,198]

membrane product is commercially available for laboratory-scale

testing, there are still many challenges and aspects that need to be
improved for the membrane to reach its full potential [120,121].
Fundamentally, aquaporin biomimetic membranes are fabricated by
combining three major components: aquaporins; which are membrane
proteins (MPs) which act as water channels; an amphiphilic housing, in
which these aquaporin proteins are reconstituted; and a porous solid
substrate, which enhances the mechanical stability. Each component is
discussed briefly in the following sections of this paper.
Fig. 5. Schematic presentation of the structure of a membrane formed by LBL
assembly and incorporating AqpZ. A layer of PEI was deposited on the H-PAN
substrate followed by PSS polyelectrolyte layer coating. Finally, aquaporin bi-
layer was fabricated by vesicle rupture.
Reprinted with permission from Wang et al.© 2015 American Chemical Society
[16].

Fig. 4. Illustration of aquaporin-embedded mixed-matrix membrane fabricated by multilayer polyelectrolyte adsorption. Hydrolyzed PAN is first functionalized with
PAH along PSS/PAA mixture, subsequently PLL-encapsulated aquaporin liposomes were deposited on them and finally again a layer of PSS/PAA was deposited on
liposomes.
Reprinted with permission from Sun et al.© 2012 Royal Society of Chemistry [176].

102
A. Fuwad, et al. Desalination 458 (2019) 97–115

Fig. 6. Schematic representation of the magnetic-aided LBL membrane fabrication process. PAH deposition onto the negatively charged H-PAN substrate (orange)
forms a polycation layer (blue). This step is followed by the deposition of a PAA-PSS mixture to form a polyanion layer (red). Next, PLL-functionalized proteopo-
lymersomes with encapsulated magnetic nanoparticles are deposited onto the polyanion layer, driven by a magnetic field. Finally, another PAA-PSS layer is added to
ensure the stabilization of the membrane. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
Reprinted with permission from Sun et al.© 2013 Royal Society of Chemistry [21].

Fig. 7. Schematic diagram of the formation of a double-layered FO membrane incorporating AqpZ. A dense layer of polyelectrolytes (PEI/PSS) was deposited on both
sides of membrane to achieve high rejection ratio.
Reprinted with permission from Wang et al.© 2015 MDPI, Basel, Switzerland [17].

Fig. 8. Diagram of nanofiltration membrane with proteoliposomes immobilized via amine-catechol bonding via pressure-assisted adsorption. Polymerized aquaporin
vesicles were stabilized on the polydopamine functionalized substrate.
Reprinted with permission from Sun et al.© 2013 Elsevier [19].

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Fig. 9. Schematic diagram of AqpZ-based biomimetic membrane preparation. The PDA functionalized aquaporin vesicles were deposited on the substrate subse-
quently a polymerized selective layer was formed using PEI.
Reprinted with permission from Li et al.© 2014 Elsevier [177].
3.1. Water channel proteins (aquaporins)
Water channels or aquaporin proteins are transmembrane proteins
with a three-dimensional structure that creates a pore allowing the
selective passage of water molecules. These proteins are present in all
three domains of life, bacteria, archaea and eukaryotes [122–126].
These proteins are important for maintaining water homeostasis in cells
and allow the transportation of water across the cell membrane. After
the first discovery of aquaporin protein in red blood cells [127,128],
aquaporins were subsequently discovered in plants, animals, and mi-
croorganisms. Aquaporins are divided into three subfamilies depending
upon their structure and functions. Aquaporins that allow only water to
pass are known as “orthodox aquaporins” [129]. Other than water,
some aquaporins also allow small molecules to pass, such as carbon
dioxide [130], urea, ammonia [131] and glycerol [131,132]; these
proteins are also known as “aquaglyceroporins” [133]. A third subclass
was recently identified and is known as “subcellular aquaporins” or
“superaquaporins” due to their unusual amino acid sequence from other
two families, but their function is still debatable because of limited
studies and difficulties in synthesis and purification [134–136].
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Desalination 458 (2019) 97–115
Fig. 10. Schematic diagram of proteopolymersome-
based polymeric biomimetic membrane. (a)
Reconstitution of dodecyl-b-D-maltoside (DDM)
AqpZ into polymersome followed by detergent re-
moval. (b) Coating of PCTE substrate. (c) & (d)
Vesicle adsorption via pressure and rupturing to
form biomimetic membrane.
Reprinted with permission from Wang et al.© 2012
John Wiley and Sons [178].
Aquaporin monomers consists of six membrane-spanning α-helical do-
mains with cytoplasmically oriented amino and carboxyl termini. These
membrane-spanning helices are represented as H1-H6 in Fig. 3 (b).
Moreover, the structure contains five interhelical loop regions (noted as
A–E) that form extracellular and cytoplasmic vestibules. The hydro-
phobic loops B and E overlap with the hydrophobic layer of the cell
membrane and form an hourglass structure, which allows the passage of
water molecules by forming short helices, denoted as HB and HE. This
overlapping is responsible for channeling in the monomer; both half
helices HB and HE, together with asparagine-proline-alanine (NPA)
motif, create an electrostatic barrier in the center of the channel
[137–139]. The upper part of the channel is formed by the H2 and H5
loops, and other half is formed by the C-terminus of the H1 and H4
loops. This configuration creates a pore size as narrow as 3 Å in dia-
meter, which is slightly greater than the diameter of a water molecule
(2.8 Å) and ultimately restricts the permeation of every molecule larger
than water [140,141]. The narrowest region in the channel is known as
the aromatic/arginine (ar/R) constriction site [142]. Along with water
transport, proton exclusion is an exceptional feature of aquaporin, and
the NPA motif plays an important role in this exclusion by allowing
A. Fuwad, et al.
Fig. 11. Illustration of PCTE membrane with immobilized proteopolymersomes. (a) Proteopolymersome preparation. (b) Adsorption of proteopolymersomes through
pressure. (c) Cysteamine coating. (d) Alternative coating of PDA-His in a LBL assembly.
Reprinted with permission from Wang et al.© 2013 Elsevier [117].
single-file permeation and hence preventing proton passage [143,144].
Aquaporin forms a tetramer [145] in the cell membrane, as shown in
Fig. 3 (a), and each monomer has an N-terminal and C-terminal tandem
repeat, represented in yellow and blue, respectively. Asterisks indicate
the formation of water pores in each monomer of this tetramer, which
facilitates water transport. While in some cases, other small uncharged
molecules (e.g., glycerol, CO2, ammonia, and urea) also pass through
the pore, the pore is completely impermeable to the charged particles
[146].
The synthesis of MPs is based on two methodologies, traditional
cell-based synthesis and cell-free protein synthesis (CFPS). The tradi-
tional synthesis methodology focuses on the overexpression of proteins,
which causes cytotoxicity due to alterations in the cellular metabolism
[147]. Under these circumstances, the transformation of protein
synthesis to CFPS seems more productive and valuable in terms of
nontoxicity, time efficiency, reduced difficulty, and scale up potential.
In CFPS, cells are lysed, which enables the in vitro synthesis of various
target proteins independent of living cell integrity [148]. A variety of
sophisticated cell-free systems have emerged as promising alternatives
to the classical cell-based protein overexpression strategies. Ad-
ditionally, a number of artificial environments can be applied to sta-
bilized proteins, such as liposomes [149], detergents [124], nanodiscs
[150] and insoluble expression [151,152]. Other than yield, lipid-pro-
tein interactions [153,154] and cost are the main concerns in these
methodologies that need to be optimized for commercial aquaporin
membrane production.
3.2. Amphiphilic housing
In biology, aquaporins are embedded within cell membranes as
integral (transmembrane) proteins [155]; in engineering applications
they therefore need to be integrated into specific amphiphilic mem-
branes (e.g., lipid bilayers or BCPs) that mimic the structure of the cell
membrane [156]. These membranes sequester the MPs from the sur-
rounding environment and act as a physical barrier [157] in targeted
applications. There are two representative materials in which aqua-
porins can be incorporated, lipids [158] and BCPs [159]. Lipids are
amphiphilic molecules, and in aqueous environments, they form
105
Desalination 458 (2019) 97–115
enclosed vesicular structures called liposomes. The charge and surface
properties of these membranes can be tuned by varying their compo-
sitions or adding different components to the mixture. After the dis-
covery of aquaporin proteins, many strategies were employed to re-
constitute them in lipid membranes, the most common of which is
detergent-based reconstitution (i.e., detergent removal, dilution or
dialysis) [160,161]. The mechanical properties of membranes, e.g.,
membrane fluidity and stability, can affect the functions of transmem-
brane proteins. These properties can be controlled using additives, such
as cholesterol [162].
In contrast to lipids, BCPs are used to mimic cell membranes by
forming polymersomes, with the enhanced stability and durability as-
sociated with polymers. The properties of BCPs (e.g., durability, per-
meation and thickness) can be controlled by selecting suitable blocks,
increasing the chain length, adding functional groups, and performing
further reactions for covalent crosslinking. In 2004, His-tagged aqua-
porin 0 was inserted into a BCP, and the protein orientation showed a
dependence on the symmetry of polymers [163]. Later, Kumar et al.
incorporated aquaporin Z (AqpZ) into ABA BCP vesicles and showed a
two-order increase in water permeation compared to commercial
membranes [119]. In another study, they investigated the incorporation
of aquaporin 0 in BCP membranes while retaining its functionality and
showed that the morphology of the proteopolymersomes can be con-
trolled by the ratio of proteins to polymersomes [164]. More recently,
Xie et al. studied the effect of BCP hydrophobic chain length on the
permeability of aquaporin and showed that a hydrophobic mismatch is
directly related to the osmotic permeability of aquaporin [165].
Both lipidic and polymeric synthetic membranes are currently being
used in biomimetic water purification systems. Recent studies have
indicated that BCP membranes have several advantages over lipid
membranes due to their high durability, ambient phase transition
temperature, low cost, better exclusion of small molecules, such as
water [166], and increased lifespan [167]. A comparison between
polymeric and lipidic membranes is given in a Table 5.
3.3. Substrates for membrane support
Both lipidic and polymeric synthetic membranes are too fragile to
A. Fuwad, et al.
Fig. 12. Schemes representing the fabrication and water purification me-
chanism of AqpZ-vesicle-imprinted membranes. (a) Schematic diagram of
AqpZ-vesicle-imprinted membrane preparation: (1) AqpZ-polymer vesicles; (2)
porous CA membrane substrate; (3) AqpZ vesicles immobilized on the porous
membrane; (4) AqpZ-vesicle-imprinted membrane; and (5) cross-section of the
AqpZ-vesicle-imprinted membrane. (b) Water purification mechanism of the
AqpZ-vesicle-imprinted membrane under pressure. Water molecules in the feed
solution penetrate the entire membrane in 3 steps: (1) passing from the feed
solution to the vesicles through the AqpZ water channel located at the polymer
bilayer facing the feed solution; (2) passing from the vesicles to the substrate
membrane through the AqpZ located at the polymer bilayer facing the substrate
membrane; and (3) penetrating the porous hydrophilic substrate membrane
into the permeate solution. Other solutes in the feed solution will be rejected by
the dense hydrophobic polymer layer surrounding the vesicles.
Reprinted with permission from Xie et al.© 2013 Royal Society of Chemistry
[118].
withstand the required hydrostatic pressure, mainly because in each
case, the membrane thickness is not greater than a few nanometers,
giving rise to the need for a solid support to ultimately increase the
membrane stability and mechanical strength. Solid supports are made
of either organic or inorganic materials with a porous structure.
Depending upon the structural design and surface properties of the
substrates, different stabilization and conjugation methodologies are
employed to obtain defect-free, robust membranes; such methods in-
clude vesicle fusion [16,17], vesicle adsorption [18], chemical cross-
linking [19], interfacial polymerization [20] and magnetic-aided ad-
sorption [21]. Among these methods, vesicle fusion is the most widely
adopted for the stabilization of membranes on a porous substrate be-
cause of its ease and minimal defect formation. Conjugation meth-
odologies depend on the structure and surface charge of both the sub-
strate and vesicles. Vesicle fusion on a solid substrate has been
106
Desalination 458 (2019) 97–115
extensively studied over the last few decades [168,169]; the basic
characteristics of a substrate that govern the formation of a bilayer were
determined to be the surface charge and hydrophilicity [170,171].
Organic substrates offer high flexibility in surface chemistry ma-
nipulations, as well as uniform pore size and high porosity, allowing the
proper evaluation of fabricated membrane performance. Additionally,
they have the ability to retain proteins as well as lipids, which supports
their application in biomimetic membranes.
Nanofiltration (NF) substrates offer higher flux than that achieved
by RO and significantly better retention than that achieved by ultra-
filtration, especially for low-molar-mass molecules, such as sugars, ions
and natural organic matter [172]. Therefore, most biomimetic mem-
branes are fabricated on an NF substrate because the substrate also
plays a very important role in separation. Moreover, the surface
roughness of NF substrates is very low, which facilitates lipid stabili-
zation and membrane formation [173]; in addition, their surface charge
can easily be tuned according to process requirements [174]. On the
other hand, conventional RO membranes cannot retain lipids or pro-
teins because of the water-permeable, rigid, polymeric top layer.
Therefore, noncovalently bonded lipidic membranes (vesicles and bi-
layers) are unable to retain their position due to the drag of water above
a certain pressure [175].
Depending upon the lipid structure and surface charge, different
substrate materials are used, such as CA, Psf, and polyacrylonitrile
(PAN), to obtain optimal results. Kaufman et al. prepared a lipid bilayer
membrane on a commercial NF polymeric membrane using a vesicle
fusion method [175]. Their work provided new insight into vesicle
fusion on a solid substrate and verified the coverage of the lipid bilayer
on two membranes, NF-270 and NF-7450. NF-270 has a negatively
charged surface because of the presence of weakly acidic COO– groups,
while NF-7450 also has an active layer composed of sulfonated Psf
containing strongly acidic SO3− groups. Although their membranes
showed good lipid bilayer coverage (~97%) at a low pH (pH 2), two
problems remain. The low pH environment may affect aquaporin pro-
teins, and the hydrophobic surface is not favorable for lipid vesicles
with a hydrophilic head. Li et al. fabricated a biomimetic membrane
under benign pH conditions, pH 7.8, using the commercial NF mem-
brane NF-270 [18]. They fabricated a bilayer membrane on both a bare
NF-270 membrane and a modified NF-270 membrane with a positively
charged lipid solution. Although they maintained the pH to preserve the
activity of aquaporin and modified the membrane surface, there were
some defects, which they found were mainly due to the surface
roughness and charge. Sun et al. further fabricated a membrane by
adopting a new approach, the layer-by-layer (LBL) adsorption of ve-
sicles to a hydrolyzed polyacrylonitrile (H-PAN) substrate, in which
hydrolysis induces the substrate surface to become negatively charged,
as shown in Fig. 4. To further modify the surface properties, especially
the hydrophilicity and surface roughness, they coated a membrane with
a polycationic layer of polyallylamine hydrochloride (PAH) along with
a mixture of polyacrylic acid (PAA) and polystyrene sulfone (PSS) as a
polyanion layer. This modification decreased the surface roughness
while increasing ion rejection [176]. The vesicles were well en-
capsulated by poly-L-lysine (PLL) using this methodology without
covalent interactions, and the membrane exhibited MgCl2 rejection >
95%. In a recent paper, Wang et al. demonstrated the fabrication of a
biomimetic membrane using the LBL assembly of a complex polyelec-
trolyte membrane (Fig. 5). Briefly, a negatively charged H-PAN mem-
brane was alternately coated with several polyelectrolyte layers of poly-
ethyleneimine (PEI) and polystyrene sulfonate (PSS). The positively
charged liposomes were ruptured on the polyanionic layer of PSS on the
modified substrate to form a lipid bilayer membrane [16].
To further improve the embedding of aquaporin vesicles and en-
hance their mechanical strength, Sun et al. developed a simple modified
technique aided by magnetic force, as shown in Fig. 6. Proteoliposomes
containing magnetic nanoparticles were immobilized between the
multilayers of polyelectrolytes on the H-PAN substrate driven by
A. Fuwad, et al.
Fig. 13. Aquaporin-based biomimetic membranes. (a) Schematic showing the synthesis of an aquaporin biomimetic membrane. (b) Conceptual model of an
aquaporin biomimetic membrane. (c) Image of a synthesized aquaporin biomimetic membrane with a surface area of > 200 cm2.
Reprinted with permission from Zhao et al.© 2012 Elsevier [20].
magnetic force. The liposomes were further stabilized by the poly-
electrolyte layers of PAH and the PAA-PSS blend [21]. Recently, Wang
et al. fabricated a double-layered FO membrane containing AqpZ via
LBL assembly to increase the water flux and antifouling capacity com-
pared to single-layered membranes (Fig. 7). Concisely, an H-PAN sub-
strate was coated with polyelectrolytes, PEI and PSS alternately on both
sides; finally, the liposomes containing aquaporin were ruptured on the
top side of the modified membrane [17]. However, the adsorption of
polyelectrolytes on the liposomes can create defects on the membrane
surface. To overcome this problem, Sun et al. modified the PAN
membrane with polydopamine (PDA), which readily reacts with amine
and thiol groups while enhancing the hydrophilicity. Methacrylate
monomers were used to crosslink the amine-functionalized proteoli-
posomes via UV illumination and were immobilized on the substrate via
amine-catechol adduct formation under pressure, as shown in Fig. 8
[19].
Similarly, Li et al. fabricated an aquaporin-based NF membrane
using polymer crosslinking. In short, proteoliposomes were decorated
with PDA because of its ability to adhere to different surfaces with or
without covalent bonding. PDA-coated proteoliposomes were stabilized
on the polyamide-imide (PAI) membrane and encapsulated by a PEI
polyelectrolyte layer formed at an elevated temperature [177], as
shown in Fig. 9, as synthetic polymeric cell membranes have many
advantages over synthetic lipidic membranes, as discussed above.
Wang et al. demonstrated the fabrication of a biomimetic membrane
based on polymersomes containing aquaporin on a polycarbonate
track-etch (PCTE) membrane. These thin membranes have a glass-like
surface with a uniform cylindrical pore distribution, which enables
them to capture particles larger than their pore size precisely. Fig. 10
represents the membrane preparation procedure. Briefly, a gold-coated
107
Desalination 458 (2019) 97–115
PCTE membrane was modified with a cysteamine monolayer through
chemisorption. The membrane was activated by EDC/NHS chemistry,
and the acrylate groups were formed by immersing the membrane in
acrylic acid. Polymersomes containing aquaporin slightly intruded into
the membrane under critical pressure, and vesicle fusion was induced
under UV illumination while covalent linkages were formed between
the methacrylate end groups of the polymersomes and the acrylate
residues on the porous substrate [178]. In another work, Wang et al.
presented a biomimetic membrane with immobilized vesicles on a gold-
coated PCTE membrane [117]. Disulfide‑gold conjugation was used to
tether the vesicles to the membrane under critical extrusion pressure.
Subsequently, the membrane was coated with a monolayer of self-as-
sembled cysteamine; then, the free spaces were covered via several
cycles of PDA-histidine coating. The scheme is shown in Fig. 11. Other
than the inherent mechanical strength of crosslinked vesicles, the dense
layers of PDA also prevent vesicle detachment from the substrate sur-
face during operation.
Xie et al. demonstrated the fabrication of a biomimetic membrane
containing aquaporin, referred to as an “aquaporin vesicle-imprinted
membrane,” via a surface imprinting technique (Fig. 12). Briefly, UV-
crosslinked polymersomes incorporating aquaporin were conjugated
onto the amine-functionalized, porous CA support by an amidation
reaction. The membrane consisted of two layers, an upper hydrophobic
polymer layer to protect the vesicles from the surroundings and a lower
hydrophilic substrate layer to allow the smooth passage of water mo-
lecules [118].
Psf substrates are known for their toughness and stability at high
temperatures and pressures and are known as superior replacements for
polycarbonate substrates. In addition, they are resistant to fouling and
have a low surface roughness. Zhao et al. fabricated an aquaporin-based
A. Fuwad, et al.
Fig. 14. Schematic of AqpZ-based hollow fiber membrane preparation (not to scale). The embedded aquaporin vesicles on inner surface of hollow fiber membrane
was encapsulated with polyamide layer.
Reprinted with permission from Li et al.© 2015 Elsevier [182].
biomimetic membrane using interfacial polymerization (Fig. 13).
Briefly, a Psf substrate was soaked in m-phenylene-diamine (MPD)
containing proteoliposomes and then exposed to trimesoyl chloride
(TMC) to form a crosslinked polyamide layer encapsulating proteoli-
posomes [20]. This process allows the scaled-up fabrication of mem-
branes (over 200 cm2) with minimal defects, and shows better perfor-
mance when tested against conventional membranes in long term
operations [179], chemical cleaning [180] and osmotic membrane
bioreactors [181].
Li et al. demonstrated the fabrication of an aquaporin-based hollow
fiber composite membrane (Fig. 14). Briefly, proteoliposomes were
108
Desalination 458 (2019) 97–115
Fig. 15. Schematic representation of the structure of a sup-
ported lipid bilayer (SLB) membrane incorporating AqpZ with
covalent bonds. Using EDC/S-NHS as the catalyst, the amide
bond-linked DOPE SLB is established on top of a porous Psf
(gray) support coated with PDA (brown). (For interpretation
of the references to color in this figure legend, the reader is
referred to the web version of this article.)
Reprinted with permission from Ding et al.© 2015 Royal
Society of Chemistry [183].
deposited on the inner surface of a polyether sulfone (PES) hollow fiber
ultrafiltration membrane by soaking in MPD solution. Subsequently, the
inner surface was exposed to a TMC solution to form a polyamide layer
with encapsulated proteoliposomes [182]. Ding et al. fabricated a
planar biomimetic membrane containing AqpZ by forming amide bonds
between lipid bilayers and a microporous Psf substrate. The membrane
configuration is illustrated in Fig. 15. A Psf substrate was modified with
a PDA layer; then, the aquaporin bilayer was stabilized via an amida-
tion reaction between the carboxyl groups of the PDA layer and the
amino groups of the proteoliposomes [183]. Table 6 summarizes the
main characteristics of biomimetic membranes on organic substrates
 A. Fuwad, et al.

Table 6
Organic substrate-based biomimetic aquaporin membranes.
Platform Substrate Conjugation method Operating condition Permeability Salt rejection LPR Area Remarks References
(cm2)

AqpZ-DOPC NF270 coated with DOTAP Pressure-assisted adsorption; charge- 1 mM NaCl @ 1 bar 3.6 LMH/bar 20% NaCl 1:200 28.26 Very low salt rejection and water [18]
induced adsorption flux, cannot be scaled up because of
defects
AqpZ-POPC/POPG/ H-PAN alternately coated with PL-coated vesicles encapsulated 200 ppm MgCl2 @ 6 LMH/bar 96% MgCl2 1:50 0.785 Very small membrane area, [176]
cholesterol polyelectrolyte films (PAH and PSS- between polyelectrolyte layers 4 bar chemicals may affect protein activity
PAA)
AqpZ-POPC/POPG/ H-PAN alternately coated with Magnet-aided vesicles encapsulated 0.3 M sucrose and 21.8 LMH 2.4 gMH 1:50 0.785 Difficult to scale up because of the [21]
cholesterol polyelectrolyte films (PAH and PSS- between polyelectrolyte layers 200 ppm MgCl2 many chemicals used and adsorption
PAA)
AqpZ-DOPC/DOTAP H-PAN alternately coated with Structure assembled LBL using 500 ppm NaCl/ 5.5 LMH/bar 75% NaCl, 97% 1:50 19.56 Chemicals can affect bilayer [16]
polyelectrolytes (PSS, PEI) electrostatic interactions and vesicle MgCl2 @ 4 bar Mgcl2 integrity and protein functions
fusion
AqpZ-DOPC/DOTAP H-PAN alternately coated with Vesicles fuses with electrostatic 2 M MgCl2 and DI 15.6 LMH 3.4 gMH 1:50 36 Large membrane area with [17]
polyelectrolytes (PSS-PEI) interactions water properties can be scaled up

109
AqpZ-DOPC PDA-treated PAN substrate Chemical crosslinking of vesicles on 200 ppm NaCl/ 3.8 LMH/bar 66.2% NaCl, 88.1% 1:100 0.785 Very small membrane area with [19]
PDA-coated membrane under MgCl2 @ 5 bar MgCl2 defects
pressure
AqpZ-ABA Gold-coated PCTE substrate Pressure-assisted disulfide and gold 6000 ppm NaCl and 17.6 LMH 91.8% NaCl 1:400 0.196 Reasonable properties but limited by [117]
conjugation with a PDA-His coating 0.8 M sucrose small area
AqpZ-ABA Gold-coated PCTE substrate Vesicle fusion by covalent 200 ppm NaCl, 16.4 LMH 90% NaCl 1:100 0.096 Too small of a membrane area with [178]
interactions under pressure 0.3 M sucrose defects
AqpZ-DOPE/DOTAP L-Dopa-modified Psf substrate Covalent bonding between PDA and 2000 ppm MgCl2 @ 6.31 LMH/bar 90% MgCl2 1:100 36 Simple coating technique can be [183]
proteoliposomes 4 bar scaled up
AqpZ-DOPC Psf substrate Vesicle encapsulation by polyamide 10 mM NaCl @ 4 LMH/bar 98% NaCl 1:200 > 200 Highest salt rejection with large [20]
layer via interfacial polymerization 10 bar area, high potential for scaling up
AqpZ-DOPC PES hollow fiber substrate Vesicle encapsulation in polyamide 500 ppm NaCl @ 55.2 LMH 97.5% NaCl 1:100 34.2 Hollow fiber system has high [182]
layer 5 bar potential for commercial use
AqpZ-ABA Amine-functionalized CA substrate Surface-imprinting technique and 200 ppm NaCl/ 22.9 LMH/bar 61% NaCl; 75% 1:200 0.196 Small area with coating defects [118]
crosslinking MgCl2 @ 5 bar MgCl2
AqpZ-DOPC PAI substrate PDA-coated vesicle immobilization 100 ppm MgCl2 @ 36.6 LMH/bar 85% MgCl2 1:400 28.3 Simple coating technique with some [177]
within PEI matrix 1 bar effects on protein activity
AqpZ-DOPC APTES-PDA functionalized PCTE Electrokinetic immobilization of 2000 ppm NaCl and 7.45 ± 0.62 LMH 97.8 ± 0.7% NaCl 1:200 0.635 Delicate coating technique offers [184]
substrate liposomes 1M sucrose high controllability and uniformity.
Desalination 458 (2019) 97–115
A. Fuwad, et al.
Fig. 16. Electrokinetic immobilization of aquaporin liposomes on the polymeric substrate. The charged aquaporin liposomes were driven under applied voltage of 1V
and stabilized on each pore.
Reprinted with permission from Fuwad et al.© 2019 Elsevier [184].
Fig. 17. Schematic representation of two biomimetic membranes on porous substrates. (a) Biomimetic membrane fabricated on porous alumina. (b) Biomimetic
membrane fabricated using a cushion and substrate coating.
Reprinted with permission from Wang et al.© 2011 Royal Society of Chemistry [186].
along with their performance. Most recently, Fuwad et al. reported an
electrokinetic immobilization technique to stabilize aquaporin lipo-
somes on a PDA functionalized PCTE substrate [184]. The aquaporin
liposomes were electrokinetically driven across the substrate and the
liposomes entrapped within or on the pores of the substrate due to the
small pore size, which ensures the uniform coating of liposomes
without any aggregation or rupture. The membrane shows high water
flux of 7.45 LMH with high desalination property of 97.8% NaCl re-
jection. Fig. 16 shows the electrokinetic coating mechanism of aqua-
porin membrane.
Inorganic substrates have advantages in terms of mechanical, che-
mical and thermal stability. Although inorganic substrates are more
expensive than their organic counterparts, they are also resistant to
solvents, have a well-defined pore structure and can be sterilized. In
addition to the aforementioned properties, alumina in particular has a
uniform pore size with a high pore density. Duong et al. functionalized
an alumina surface with gold and deposited a polymeric bilayer using
covalent interactions between the gold- and disulfide-functionalized
ends of polymeric vesicles [185]. Although the membrane pore size was
uniform with a high porosity, due to the large pore size (55 nm), some
defects formed in the membrane bilayer. To protect the transmembrane
proteins from becoming denatured by contact with the support surface,
Wang et al. proposed the idea of a polyethylene glycol (PEG) cushion
supported by alumina, as shown in Fig. 17. Briefly, PEG molecules
where chemisorbed onto gold-coated alumina by thiol interactions, and
the vesicles were subsequently ruptured on the PEG-cushioned alumina
substrate [186]. Data regarding inorganic substrates are summarized in
110
Desalination 458 (2019) 97–115
Table 7. However, the utilization of inorganic substrates in aquaporin
membranes remains limited.
3.4. Advantages of biomimetic membranes
Fouling is a problem that all membrane technologies must address.
The lack of isoporosity is one cause of fouling in the conventional
membranes; they have a wide pore size distribution, allowing the per-
meation of species that should be retained as well as inappropriate
initial flux that blocks pores [23,187]. Another major issue is achieving
high flux with low-pore-density membranes. Usually, all conventional
membranes have a low pore density due to the inherent nature of the
fabrication material and manufacturing technique [188].
Due to its inherent structural properties, aquaporin is the solution to
a number of unsolved issues presented by conventional membranes.
Biomimetic membranes can easily overcome the aforementioned gen-
eric issues of conventional technologies. The aquaporin structure pos-
sesses a uniform pore size that prevents the blockage of pores by un-
wanted species, rendering the membranes resistant to fouling [182].
Fig. 18 illustrates the generic problems of conventional membranes and
the advantages of aquaporin.
3.5. Challenges that biomimetic membranes must overcome
There are several challenges that must be addressed for biomimetic
membranes to become an industrially appropriate tool for water pur-
ification. First, the production of aquaporin proteins is central to the
A. Fuwad, et al. Desalination 458 (2019) 97–115

success of these membranes, but the purity and quantity of these hy-
References
drophobic MPs cannot easily be controlled due to their narrow range of

[185]

[186]
stability in a defined aqueous environment that requires the presence of
a specialized detergent. Second, the most important challenge is their

Increased mechanical stability of biomimetic membrane by the

Very low water permeability, salt rejection and small membrane
intact and functional reconstitution into artificial systems. Although
lipid and BCP-based structures are the ideal analogues to biological
cells, the resulting membranes lack the necessary mechanical stability
because they are only a few nanometers thick. The third critical chal-
lenge is the upscaling of aquaporin membrane fabrication. The uniform
coating of proteins on an industrial-scale membrane substrate is still
very difficult to attain because conventional coating methodologies
borrow chemical conjugation and pressure driven immobilization,
which results in many defects during fabrication. Therefore, a delicate
application of PEG as a cushion

method is required for uniform coverage of aquaporin membranes on

solid substrates having industrial scalability.

4. Conclusions and future outlook

There are several potential emerging approaches to improving

Remarks

aquaporin integrity and stability for long-lasting industrially applicable

area

membranes. For instance, nanolipoprotein particles (NLPs) can be one

option to overcome current limits to protein stability and incorporation
(cm2)
Area

efficiency. This technique can synthesize and incorporate the aquaporin

n/a
0.2

protein in an in vitro format without the use of detergents and other

1:2000

aqueous environments that may harm proteins' activity and proper

1:50
LPR

folding. 3D bio-printing is another emerging potential technique for

fabricating defect free aquaporin membranes, although it is currently
Salt rejection

45.1% NaCl

being utilized only for tissue and organ research. However, continuous
development will lead from organ printing to mimicking complex
membrane structures to in situ fabrication of micro 3D environments.
n/a

Aquaporin, like other membrane proteins, must be integrated

8.2 LMH/bar
Permeability

within amphiphilic materials, either lipids or synthetic materials, such

as BCPs. Currently, research is being carried out to study the interac-
tions between the amphiphilic housing (lipid, BCP) and proteins, such
n/a

as those involved in lipid mobility, and their effects on protein func-

Operating condition

tions. Particularly hydrophobic region length matching with aquaporin

200 ppm NaCl @

is the major barrier to aquaporin's stability and functionality. The

limitation on amphiphilic housing thickness to only a few nanometers
margin preclude the commercial success of aquaporin membranes.
5 bar

Unfortunately, the progress in this area is sluggish owing to the lack of

n/a

available materials other than BCPs to replace lipids. Successful im-

plementation of in vitro use of aquaporin membranes can be achieved
Vesicle rupture with disulfide‑gold

only by developing materials that mimic biological membranes with

Vesicle rupture on PEG cushion

superior stability in a few nanometer scales, while the inherent in-

stability of membranes can be ameliorated by giving an additional
Immobilization method

supporting layer to the aquaporin membrane.

Aquaporin biomimetic membranes developed to date are fabricated
Inorganic substrate-based biomimetic aquaporin membranes.

on conventional porous solid substrates. The substrates used to support

conjugation

aquaporin membranes were proposed on empirical approaches, which

has not significantly advanced the performance of aquaporin mem-
branes. As recent studies showed that water purification capabilities
highly rely on the structure of solid substrates, by giving additional
functional layers researchers have focused on finding a better substitute
PEG-functionalized, gold-coated

of the supporting materials and interfacing them to aquaporin mem-

branes.
The most likely near-term niche for biomimetic aquaporin mem-
Gold-coated alumina

branes in water treatment is FO applications. In this emerging tech-

nological space, there is a lot of room for innovative membrane mate-
rials. FO is a natural application for aquaporin membranes because
Substrate

alumina

aquaporin essentially plays a forward osmosis-based separation func-

tion in nature. For other membrane technologies like RO, successful
market entry requires several challenges to be addressed, including
AqpZ-DMPC

long term stability and robustness under harsh operating and cleaning
AqpZ-ABA
Platform

conditions. Successful integration of biological and non-biological

Table 7

components may lead to a platform having the efficiency and specificity

of biological systems such as the kidney.

111
A. Fuwad, et al. Desalination 458 (2019) 97–115

Fig. 18. Illustration of (a) the disadvantages of conventional membranes, due to their inherent structural characteristics low flux and fouling are the major problems
(b) the advantages of aquaporin membranes over traditional membranes. Water transport is mediated by selective diffusion due to osmotic gradient. Hourglass shape
along with selective extracellular and intracellular vestibules allows water molecules while ejecting impurities.

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