Article Cite This: Acc. Chem. Res. 2018, 51, 1082−1091
pubs.acs.org/accounts
Bioinspired Materials for Controlling Ice Nucleation, Growth, and Recrystallization Zhiyuan He,†,‡ Kai Liu,†,‡ and Jianjun Wang*,†,‡ †
Key Laboratory of Green Printing, Institute of Chemistry, Chinese Academy of Sciences, Beijing 100190, China School of Chemistry and Chemical Engineering, University of Chinese Academy of Sciences, Beijing 100049, China
‡
CONSPECTUS: Ice formation, mainly consisting of ice nucleation, ice growth, and ice recrystallization, is ubiquitous and crucial in wide-ranging fields from cryobiology to atmospheric physics. Despite active research for more than a century, the mechanism of ice formation is still far from satisfactory. Meanwhile, nature has unique ways of controlling ice formation and can provide resourceful avenues to unravel the mechanism of ice formation. For instance, antifreeze proteins (AFPs) protect living organisms from freezing damage via controlling ice formation, for example, tuning ice nucleation, shaping ice crystals, and inhibiting ice growth and recrystallization. In addition, AFP mimics can have applications in cryopreservation of cells, tissues, and organs, food storage, and anti-icing materials. Therefore, continuous efforts have been made to understand the mechanism of AFPs and design AFP inspired materials. In this Account, we first review our recent research progress in understanding the mechanism of AFPs in controlling ice formation. A Janus effect of AFPs on ice nucleation was discovered, which was achieved via selectively tethering the ice-binding face (IBF) or the non-ice-binding face (NIBF) of AFPs to solid surfaces and investigating specifically the effect of the other face on ice nucleation. Through molecular dynamics (MD) simulation analysis, we observed ordered hexagonal ice-like water structure atop the IBF and disordered water structure atop the NIBF. Therefore, we conclude that the interfacial water plays a critical role in controlling ice formation. Next, we discuss the design and fabrication of AFP mimics with capabilities in tuning ice nucleation and controlling ice shape and growth, as well as inhibiting ice recrystallization. For example, we tuned ice nucleation via modifying solid surfaces with supercharged unfolded polypeptides (SUPs) and polyelectrolyte brushes (PBs) with different counterions. We found graphene oxide (GO) and oxidized quasi-carbon nitride quantum dots (OQCNs) had profound effects in controlling ice shape and inhibiting ice growth. We also studied the ion-specific effect on ice recrystallization inhibition (IRI) with a large variety of anions and cations. All functionalities are achieved by tuning the properties of interfacial water on these materials, which reinforces the importance of the interfacial water in controlling ice formation. Finally, we review the development of novel application-oriented materials emerging from our enhanced understanding of ice formation, for example, ultralow ice adhesion coatings with aqueous lubricating layer, cryopreservation of cells by inhibiting ice recrystallization, and two-dimensional (2D) and three-dimensional (3D) porous materials with tunable pore sizes through recrystallized ice crystal templates. This Account sheds new light on the molecular mechanism of ice formation and will inspire the design of unprecedented functional materials based on controlled ice formation.
1. INTRODUCTION
and chemical industries. On the other hand, these materials can feed back to new experimental data, allowing theorists to reconsider the understanding of ice formation.9,11,13 In this Account, we will first summarize our understanding of the mechanism by which AFPs control ice formation, focusing on the Janus effect of AFPs and its molecular origin. In the following three sections, we will discuss the design and synthesis of AFP mimics in tuning ice nucleation, controlling ice shape and growth, and inhibiting ice recrystallization. Then, we will present some applications of materials that are capable of controlling ice formation, such as the fabrication of and anti-ice coating with an aqueous lubricating layer, cryopreservation of horse sperm utilizing 2D nanosheets, and preparation of 2D and 3D porous
In nature, some plants, insects, and fishes produce antifreeze proteins (AFPs) to control ice formation so that they can survive in subzero environments.1−3 AFPs can depress the freezing temperature and achieve a temperature difference between the freezing and melting temperatures of ice, which is termed as thermal hysteresis (TH).4 The adsorption of AFPs causes microcurvatures on the ice surface between adjacent AFPs, thereby depressing the further growth of ice due to the Kelvin effect.5 AFPs also have a pronounced effect on ice recrystallization inhibition (IRI), that is, the growth of large ice crystals at the expense of small ones.6 Inspired by the unique functions of AFPs on shaping ice crystals and inhibiting ice growth and recrystallization,7,8 rich varieties of materials have been developed to control ice formation.9−12 On one hand AFPs inspired materials are essential for practical applications in food, pharmaceutical, © 2018 American Chemical Society
Received: October 23, 2017 Published: April 17, 2018 1082
DOI: 10.1021/acs.accounts.7b00528 Acc. Chem. Res. 2018, 51, 1082−1091
Article
Accounts of Chemical Research
Figure 1. Janus effect of antifreeze proteins on ice nucleation. (A) Selectively binding the IBF and the NIBF of AFPs to solid substrates. (B) Effects of the NIBF and IBF surfaces on the ice nucleation temperature. (C) Side view and (D) top view of water molecules atop the IBF. (E) Side view and (F) top view of water molecules atop the NIBF (carbon, nitrogen, oxygen, and hydrogen atoms are represented in cyan, blue, red, and white spheres, respectively).
groups and hydrophilic hydroxyl groups (Figure 1C,D). In contrast, no ordered water structure has been observed atop the NIBF, which is attributed to the irregular array of hydrophobic/ hydrophilic groups and the presence of hydrophobic and charged groups (Figure 1E,F). Further analysis reveals that ice nucleation is energetically favored to occur on the top of the IBF with ordered ice-like structure, while liquid water tends to be in contact with the NIBF. When the AFPs are freely distributed in body fluids, the IBF binds preferentially to the basal or prism plane of ice crystals and the NIBF faces liquid water (Figure 2A).17 The binding of IBF results in microcurvatures on the ice surface between AFPs; as a result, further growth of ice crystals is inhibited owing to the Kelvin effect.18 The shaping effect and TH activity of AFPs both stem from their ability to bind to ice with the IBF (Figure 2B−E).4,7 In our investigation, we have discovered a correlation between the activity of different types of AFPs on ice nucleation and that on the TH gaps, that is, hyperactive AFPs with large TH gaps exhibit higher activities in tuning ice nucleation and moderately active AFPs with small TH gaps show lower activities in regulating ice nucleation. For hyperactive MpAFP, the difference between ice nucleation temperatures on IBF and NIBF modified surfaces is about 9 °C; whereas for moderate type III AFP, the difference is only 2 °C.13 A snapshot of the MD simulation in Figure 2F shows that the disordered interfacial water layer atop the NIBF hinders the overgrowth of ice on the AFP, which is indicated by the curvature on the ice surface. AFPs with various
materials with tunable pore sizes. Finally, we will give a brief conclusion and perspective.
2. MECHANISM OF REGULATING ICE FORMATION BY ANTIFREEZE PROTEIN AFPs have the unique capability to control ice formation via adsorbing to the surface of ice crystals.7 The possible contributions of hydrogen bonding and hydrophobic effects were studied for the mechanism by which AFPs bind to ice.4,14 Both have the same precondition, that the ice-binding face (IBF) of AFPs matches the basal or prism plane of ice to which they bind.7 Recently, a number of studies found that the IBF of AFPs organizes interfacial water molecules into an ice-like arrangement, which may facilitate the merger of AFPs with ice.15,16 However, whether the non-ice-binding face (NIBF) contributes to the functions of AFPs remains unknown.13 In our recent study, IBF and NIBF of AFPs from Microdera puntipennis dzungarica (MpdAFP), a beetle inhabiting in Xinjiang province of China, were selectively tethered to solid substrates (Figure 1A), and the effects of different faces of AFPs on ice nucleation were studied as shown in Figure 1B.13 The assays show that ice nucleation is facilitated if the IBF is exposed to liquid water, whereas ice nucleation is inhibited when the NIBF is in contact with liquid water. Further molecular dynamics (MD) simulations show that the water molecules on the top of the IBF display an ordered hexagonal ice-like structure, which is attributed to the combined action of specific spatial arrangement of hydrophobic methyl 1083
DOI: 10.1021/acs.accounts.7b00528 Acc. Chem. Res. 2018, 51, 1082−1091
Article
Accounts of Chemical Research
Figure 2. (A) Proposed mechanism of AFPs for ice growth inhibition. (B, C) Shape of a single ice crystal in an MpdAFP solution viewed along the a and c axes, respectively. (D) The shape of a single ice crystal in a 20 mM Tris buffer is shown for comparison. (E) TH values of the MpdAFP solution with various concentrations. (F) A typical side view snapshot of the simulation result with the IBF of TmAFP in contact with ice. The curved ice crystal surface is highlighted by the blue dash lines.
delayed for 1974 s on the surface modified with E36. Our theoretical analysis shows that the asymmetric polarization of interfacial water on positively and negatively charged SUP surfaces changes the energy barrier of ice nucleation, therefore positively charged surfaces promote heterogeneous ice nucleation and negatively charged surfaces inhibit it. Ionic surfaces are ubiquitous, and ice nucleation on ionic surfaces is of great importance in a wide range of biological interfaces and atmospheric aerosols.27 Although some recent reports have demonstrated that ions on ionic surfaces are able to control the dynamics and structure of interfacial water, it remains to be experimentally verified whether ions influence heterogeneous ice nucleation.28 We investigated the effect of ions on ice nucleation utilizing polyelectrolyte brush (PB) surfaces based on the following unique properties: (1) a fraction of counterions will be released from the PB to form a thin diffusion layer of counterions at the brush/water interface when a drop of pure liquid water is placed atop PB surfaces; (2) counterions of the PB can be reversibly exchanged (Figure 4A). Ice nucleation was studied on the cationic poly[2-(methacryloyloxy)-ethyltrimethylammonium] (PMETA) and anionic poly(3-sulfopropyl methacrylate) (PSPMA) brush surfaces with a series of counterions. We found that the efficiency of different ions in regulating ice nucleation agrees with the Hofmeister series (Figure 4B).29 It was further demonstrated that the heterogeneous ice nucleation temperature is tunable over a window of almost 8 °C via changing the grafting density and thickness of polyelectrolyte brushes.27 By performing MD simulation of the PB/water interface with different counterions and correlating the fraction of ice-like water molecules with the kinetics of structural transformation from liquidlike to ice-like water molecules (Figure 4C,D), we have successfully explained the mechanism of experimentally observed ionspecific effects on heterogeneous ice nucleation.
activities shall differ in degree of disorder of the interfacial water atop the NIBFs, that is, the entropy of the interfacial water differs on the NIBFs of various AFPs. The higher the entropy of the interfacial water layer atop the NIBF is, the more difficult it is for ice to overgrow that NIBF. Consequently, it provides another molecularlevel aspect of different types of AFPs possessing different TH gaps, in addition to the binding of AFPs to different ice faces.19,20
3. TUNING ICE NUCLEATION Particular interest has been focused on the effects of AFPs on ice nucleation because it is the initial step of ice formation.21 However, there were some contradictions regarding the role of AFPs on ice nucleation; for example, it was reported that a high concentration AFP solution enhanced ice nucleation, whereas it was also found that AFPs inhibited ice nucleation.22−25 Through selectively investigating the effects of IBF and NIBF of AFPs on ice nucleation, we discovered that IBF facilitates ice nucleation, while NIBF depresses ice nucleation; moreover, we also found that AFPs regulate ice nucleation through the control of interfacial water. Therefore, we prepared surface materials with tunable properties of interfacial water for controlling ice nucleation.26,27 We modified solid surfaces with supercharged unfolded polypeptides (SUPs) as shown in Figure 3A. Ice nucleation was tuned by absolutely controlling both surface charge and charge density via genetic engineering.26 The results show that SUPs with positively charged residues of lysine (K) facilitate ice nucleation, while SUPs with negatively charged residues of glutamic acid (E) suppress it (Figure 3B). The effect of charge density on ice nucleation shows that increasing charge density for negatively charged SUPs inhibits ice nucleation, whereas increasing charge density for positively charged SUPs promotes it. In order to consolidate the capability of SUPs in tuning ice nucleation, we further studied the corresponding ice nucleation delay time (Figure 3C), which is the time interval between the time when the surface modified by K36 and E36 at −19.0 °C contacts water and that when the ice nucleation occurs. Ice nucleation occurred on the surface modified with K36 within a short delay time of 54 s; in strong contrast, nucleation was
4. CONTROLLING ICE SHAPE AND GROWTH AFPs are believed to control the ice shape and growth by adsorbing to the basal or prism plane of ice crystals.4,18 Simulation analysis showed that AFPs can order water molecules into 1084
DOI: 10.1021/acs.accounts.7b00528 Acc. Chem. Res. 2018, 51, 1082−1091
Article
Accounts of Chemical Research
Figure 3. Tuning ice nucleation on supercharged unfolded polypeptide (SUP) modified surfaces. (A) The positively charged lysine and negatively charged glutamate in SUPs are represented by blue and red colors, respectively. (B) Charge density dependence of the ice nucleation temperature on the surfaces modified with a series of positively and negatively charged SUPs. The net charge density subjects to the order of K36 = E36 > HC-K30 = HC-E35 > KE16 > ELP90. Error bar is the standard error of the mean (SEM), which describes the uncertainty of how the sample mean represents the population mean. (C) Ice nucleation delay times on the surfaces modified by K36 and E36. Adapted with permission from ref 26. Copyright 2016 John Wiley & Sons.
an ice-like structure, which might facilitate the preferred binding of AFPs to the ice crystal surface.16 Recently, Davies et al. discovered experimentally that a network of ordered water forms on the AFP surface, which matches the ice lattice of both basal and prism planes.3,15 Note that ice-like water structure forms on top of the basal plane of graphene oxide (GO) surface due to the scaffold of the graphene sheet as schematically illustrated in Figure 5A.30 Interestingly, GOs of various sizes can be fractionated via controlled freezing, consolidating the binding of GOs to the surface of ice.31 We therefore investigated the growth of ice crystals in a GO dispersion. The average size of GO is around 500 nm. The carboxyl groups locate at the periphery of GO, whereas hydroxyl and epoxy groups are mainly on the basal plane of GO (Figure 5A). A profound effect of GO in controlling ice shape was revealed, that is, a hexagonal-shaped ice crystal was observed (after 240 s) in the GO dispersion at −0.4 °C, whereas a flat disc-shaped ice crystal was observed in the aqueous solution without GO (Figure 5B). Interestingly, the ice crystal in the aqueous dispersion with GOs did not show obvious growth in 2 h, while the one in the aqueous solution without GOs grew quickly, and the whole observation window was full of ice within 2 s. The investigation on the effect of the carbon to oxygen ratio (C/O) shows that the ice growth rate decreases with the decreasing C/O ratio (Figure 5C). The increase of the C/O ratio is equivalent to the reduced density of hydroxyl groups on the basal plane of GO and the increase of the hydrophobic graphite region. All the GO flakes with various C/O ratios have the same size (500 nm). The MD simulation shows that the ordered ice-like water layer atop the GO facilitates the formation of more hydrogen bonds with the ice crystal than those forming with liquid water (Figure 5D). For comparison, the inset of the Figure 5D also shows the number of hydrogen bonds formed between carboxyl-functionalized graphene (GCOOH) and ice and water. It can be seen that liquid water forms more hydrogen bonds with GCOOH and therefore
GCOOH did not exhibit obvious effects in inhibiting ice growth and shaping ice crystals.30 One can conclude that the hydrogen bonding but not the hydrophobic interaction is the key for the preferred binding of GO to the ice crystal surface. We also studied the effect of the structure match between 2D materials and the lattice of ice crystals on the ice growth. Different types of graphitic carbon nitride (g-CN) derivatives including oxidized g-CN quantum dots (OCNs) and oxidized quasi-carbon nitride quantum dots (OQCNs) were prepared.32 Figure 6A shows the differences of the in-plane structure between the OCNs and OQCNs, that is, the atomic spacing between two adjacent tertiary N atoms, which can form hydrogen bonds with O atoms of the ice crystal. For comparison, the atomic spacing between the oxygen atoms on the prism plane of ice along the c-axis is also shown side-by-side. On the OCN, the distance is ca. 7.13 Å, while it is ca. 7.42 Å on the OQCN, displaying a smaller mismatch (ca. 0.95%).32 It is found that OQCNs have an obvious capability in shaping ice crystals and inhibiting ice growth (Figure 6B). Interestingly, the sudden increase of the growth along the a-axis of the ice for the OQCN dispersion can be observed when the supercooling temperature (ΔT) increases to 0.10 °C, which is analogous to the sudden burst growth behavior of ice in AFP solutions.20 The ice growth behaviors at various ΔT further indicate that all types of OQCNs possess TH activity (Figure 6C). In strong contrast, OCNs are not capable of controlling ice shape and growth, and no TH activity is observed. We performed a modified ice affinity experiment, which was first reported by Davies et al. for the purification of AFPs via controlled ice growth on a cold finger to avoid constitutional freezing.33 We observed adsorption equilibriums on OQCNs, while no adsorption equilibrium can be found on OCNs (Figure 6D). Therefore, we propose that the binding of OQCNs to the ice leads to curvatures on the ice crystal, which suppress the further growth of ice owing to the Kelvin effect (Figure 6E). Meanwhile, 1085
DOI: 10.1021/acs.accounts.7b00528 Acc. Chem. Res. 2018, 51, 1082−1091
Article
Accounts of Chemical Research
Figure 4. (A) Illustration of tuning ice nucleation on cationic and anionic PB surfaces with different counterions. (B) Distinct efficiency of anions and cations in tuning ice nucleation follows the Hofmeister series. (C) The fraction of ice-like water molecules and the interplay between hydrogen bond making rate constant (k) and breaking rate constant (k′) of ice-like water at the brush/water interfaces. (D) Kinetics of structural transformation between liquid-like and ice-like water molecules at the brush/water interface.
system to avoid false positives.30,34,35 We discovered ion specificity in regulating ice recrystallization.36 The polarized optical microscopy images show the ice grains obtained from pure water, NaF, NaBr, and NaI aqueous solutions, indicating that the average grain size of ice crystals can be regulated to be either much larger than, comparable to, or much smaller than those obtained from pure water by simply changing the type of ions (Figure 8A). Further, we investigated the ion-specific effect on IRI activity with a large variety of anions and cations (Figure 8B,C). The mean grain size of ice crystals increases in the anion sequence HPO42− < SO42− < F− < AC− < SCN− < ClO4− < Br− < Cl− < NO3− < I− and in the cation sequence NH4+ < Mg2+ < Ca+ < Li+ < TMA+ < Na+ < Gua+ < K+ < Cs+. Our MD simulation analysis revealed that the ability of the ion to be incorporated into ice determines the ultimate size of recrystallized ice crystals. This study implied that the adsorptioninhibition mechanism is not the only mechanism affecting the IRI. At the same time, it is worth mentioning that the type of ions employed during the evaluation of the activity of an ice recrystallization inhibitor, as such the activity of ice recrystallization inhibitors, can be compared from different groups worldwide.
the structure match plays a critical role in the preferred adsorption of 2D materials on the ice crystals.
5. INHIBITING ICE RECRYSTALLIZATION Preferred adsorption of AFPs onto the ice crystal surface endows the AFPs with the IRI activity.6 It was found that a concentration as low as micromolar is needed for the IRI activity of AFPs.7 Inspired by AFPs, a number of synthetic IRI-active materials have been developed to meet the need for practical applications.11,12 In our group, quantitative evaluation of the IRI activities of GO was investigated via a “splat-cooling” assay, that is, polycrystalline ice formed after a droplet of 10 μL of a GO dispersion was dripped from a height of 1.5 m onto a precooled cover glass with surface temperature of −60 °C, and then the sample was annealed at −6 °C for 30 min.30 Figure 7A displays typical optical microscopic images of recrystallized ice crystals from NaCl aqueous solutions (8.0 mg mL−1) with and without GO. The addition of GO could reduce the average grain size of recrystallized ice by more than 1 order of magnitude. Note that at a low concentration of 0.01 mg mL−1, GO shows higher IRI activity than poly(vinyl alcohol) (PVA), which is reported to be an effective AFP mimic (Figure 7B).11 During the IRI experiments, an adequate amount of salts, for example, phosphate-buffered saline (PBS) solution or NaCl solution, is needed to ensure that liquid is present in the recrystallization
6. APPLICATIONS Controlling ice formation can find broad applications in food, pharmaceutical, and chemical industries, and here we give three 1086
DOI: 10.1021/acs.accounts.7b00528 Acc. Chem. Res. 2018, 51, 1082−1091
Article
Accounts of Chemical Research
Figure 5. Controlling ice shape and growth with GO. (A) Arrangement of oxidized groups on the basal plane of GO matches the lattice parameter of ice crystal. (B) Effects of GO on the growth and shape of ice crystal. (C) Ice growth rates in GO dispersions with GO of the same size (500 nm) but various C/O ratios. (D) Snapshot of the MD simulation shows the formation of an ice-like water layer atop GO. The atoms are colored as follows: C, cyan; O, red; H, white, oxygen of water molecules forming hydrogen bonds with hydroxy groups of GO, green. Inset shows the average number of hydrogen bonds between the oxidized groups on the basal plane of GO (or GCOOH) and water or ice. Adapted with permission from ref 30. Copyright 2017 John Wiley & Sons.
examples for demonstration, construction of anti-icing coatings, cryopreservation of cells and tissues, and fabrication of 2D and 3D porous materials. Undesired ice accumulation on solid surfaces could cause serious problems such as extra energy consumption, infrastructure damage, and loss of lives in extreme cases, and current strategies for anti-icing are often energyconsuming, high-cost, and environmentally harmful.37,38 An ideal anti-icing coating would reduce the adhesion of ice to the surface such that ice formed atop can be shed off due to the action of wind or its own gravity.37 Because of the existence of the lubricating water layer, the adhesion between the skate blade and ice is reduced substantially. Therefore, people can skate on ice with grace (Figure 9A).39 Inspired by ice skating, we have invented ultralow adhesion anti-icing coatings with an aqueous lubricating layer.40 The temperature window in which the aqueous lubricating layer exists can be adjusted by tuning the chemistry of hygroscopic polymers in the lubricating layer, that is, the structure and dynamics of the confined water layer can be controlled by the chemistry of hygroscopic polymers.38,40 It was found that such an anti-icing coating was able to maintain ultralow ice adhesion at temperatures down to −53 °C (Figure 9B), and ice on the top of the coating could be shed off by the action of a strong wind (10−12 m/s) (Figure 9C). For the cryopreservation of cells and tissues, ice recrystallization during thawing is accompanied by dehydration and structural damage to cells.7 As AFPs have obvious IRI activity, it was reported that AFPs can be used as cryoprotectant.11,41 However, some groups discovered the decrease of cell recovery in AFP solutions possibly due to their potential cytotoxicity and iceshaping effect.42 Moreover, the difficulty in large-scale synthesis of AFPs also limited their applications for cryopreservation.35
Therefore, development of effective synthetic ice recrystallization inhibitors as cryoprotectants has been continuously pursued.9,11,35 Noting that GO can inhibit ice recrystallization at a very low concentration (Figure 7B), we utilized GO as a cryoprotectant for horse sperm cells. The optical microscopy images in Figure 10A show the sperm cell membrane integrity after freezing−thawing, and the cell membrane integrity with conventional cryoprotectants is also shown side-by-side for comparison.30 It can be clearly seen that the number of abnormal horse sperm (highlighted by yellow circles) is reduced significantly with GO as the cryoprotectant. Moreover, the ratio of motile cryopreserved horse sperm is increased from 24% to 72% with the addition of only 0.01 wt % GO (Figure 10B). Though this result opens a new avenue for the application of 2D materials, careful verification of 2D materials for the cryopreservation of other cells needs to be carried out. An interesting feature of ice recrystallization is that the additives are excluded from ice and left between the grains.43 Ice can be removed by sublimation, leaving templated porous material.36 In addition to the well-studied ice templating methods such as freeze-casting and ice-segregation-induced self-assembly, recrystallized ice can provide a unique approach for the fabrication of porous materials with controllable pore sizes.44−46 Recrystallized ice crystals are utilized as templates to fabricate porous materials. 2D and 3D porous structures with tunable pore sizes can be obtained (Figure 11A,B).36 This approach is applicable to almost all types of materials ranging from inorganic salts, biopolymers, quantum dots, and metallic particles to polymer colloids (Figure 11C).
7. CONCLUSION AND PERSPECTIVE This Account reviewed our recent progress on understanding and controlling ice formation. We discovered the Janus effect of 1087
DOI: 10.1021/acs.accounts.7b00528 Acc. Chem. Res. 2018, 51, 1082−1091
Article
Accounts of Chemical Research
Figure 6. Controlling ice shape and growth with OQCNs. (A) Possible in-plane structures of OCNs, OQCNs, and primary prism face of hexagonal ice. (gray spheres) O atoms; H atoms have been omitted for clarity; (dotted circle) O atoms in another layer being 0.92 Å behind those in the paper plane. (B) Growth processes of single ice crystal in OCNs and OQCNs-180-3 aqueous dispersions. (C) The growth rates of ice crystals in various samples under different ΔT. All the sample concentrations are 4.0 mg mL−1. (D) Modified ice affinity experiment results. (E) Proposed mechanism of OQCNs on regulating the growth and shape of ice crystals. Adapted with permission from ref 32. Copyright 2017 John Wiley & Sons.
Figure 7. IRI activity of GO. (A) Microscopic images of ice crystals grown in NaCl aqueous solution of 8.0 mg mL−1 with and without GO (5 mg mL−1, 500 nm in size) after annealing at −6 °C for 30 min; insets are the grain size distributions. (B) Distribution of grain sizes of ice crystals obtained in NaCl aqueous solution of 8.0 mg mL−1 with GO and PVA. The concentration of GO and PVA is 0.01 mg mL−1. Adapted with permission from ref 30. Copyright 2017 John Wiley & Sons.
AFPs on ice formation, and our investigation on the mechanism of AFPs at the molecular level revealed that interfacial water
plays a critical role. Further design and fabrication of AFP mimics reinforced the importance of the interfacial water on the 1088
DOI: 10.1021/acs.accounts.7b00528 Acc. Chem. Res. 2018, 51, 1082−1091
Article
Accounts of Chemical Research
Figure 8. Ion-specific effect on ice recrystallization. (A) Microscopic images of recrystallized ice crystals grown in pure water, NaF, NaBr, and NaI aqueous solutions, respectively. A more complete series of (B) anions and (C) cations in tuning ice recrystallization.
Figure 9. (A) Schematic drawing of the anti-icing coating with aqueous lubricating layer inspired by ice skating (the painting in the top left is Ice Skating, by Hy Sandham 1885, courtesy of the Library of Congress). Adapted with permission from ref 39. Copyright 2014 John Wiley & Sons. (B) The solid line is the ice adhesion strength, and the dashed line is differentiated from the solid line. Regimes I−III represent the aqueous lubricating layer disappearing with the decrease of the temperature. (C) Effectiveness of the anti-icing coating with an aqueous lubricating layer was tested in the wind tunnel. The ice on the coating can be blown off with a strong breeze. Thick arrows denote the direction of the wind. Adapted with permission from ref 40. Copyright 2014 American Chemical Society. 1089
DOI: 10.1021/acs.accounts.7b00528 Acc. Chem. Res. 2018, 51, 1082−1091
Article
Accounts of Chemical Research
Figure 10. Application of GO nanosheets for cryopreservation. (A) The integrity of sperm cell membranes of horse sperm after freeze−thawing with various cryoprotectants, glycerol, GCOOH, and GO, compared with those in culture medium. The damaged sperm cells are highlighted by yellow circles showing that the tail of the sperm is missing, and unimpaired sperm are highlighted by green circles. (B) The ratio of motile cryopreserved horse sperm with different cryoprotectants. Adapted with permission from ref 30. Copyright 2017 John Wiley & Sons.
structure and dynamics of interfacial water and molecular structure of various types of AFPs with different capabilities in controlling ice formation. On the other hand, it demands continuous efforts to study more systems in nature, such as ice nucleating proteins and saccharides, possessing unique capabilities in controlling ice formation. As such, the secret of puzzling yet critically important ice formation can be unveiled.
■
AUTHOR INFORMATION
Corresponding Author
*E-mail:
[email protected]. ORCID
Jianjun Wang: 0000-0002-1704-9922 Notes
The authors declare no competing financial interest.
Figure 11. Various porous materials prepared with recrystallized ice crystals as the template. (A) Size of the 2D meshes can be easily regulated by changing the type of ions (F−, Br−, and I−, 0.01 M) in the recrystallizing aqueous solution. (B) 2D and 3D porous materials can be prepared with recrystallized ice crystals as the template. (C) Various materials such inorganic salts, collagen, quantum dots, metallic nanoparticles, and polystyrene colloids can be used to prepare porous materials.
Biographies Zhiyuan He received his Ph.D. at Institute of Chemistry, Chinese Academy of Sciences (ICCAS), in 2014. Currently he works as an associate professor at ICCAS. His research interest is the fabrication and application of polymeric anti-icing materials. Kai Liu joined Prof. Jianjun Wang’s group and received his M.S. degree in 2013. He is currently a Ph.D. candidate at ICCAS.
nucleation, growth, shaping, and recrystallization of ice crystals. Moreover, we also discussed application-oriented materials relying on our enhanced understanding of ice formation, that is, aqueous lubricating anti-icing coatings, cryopreservation of cells, and templates for porous materials with recrystallized ice. The continuously increasing applied aspects of ice demand molecular level understanding of ice formation. Although ice has attracted the interests of scientists for hundreds of years, the molecular level mechanism of ice formation still puzzles us. Learning from nature may provide new ideas. Unravelling the mechanism of AFPs is just one example to bring new aspects of ice formation. Despite current successes, much work remains in this challenging field. On one hand, more in-depth understanding of AFPs in controlling ice formation waits to be accomplished both experimentally and theoretically. For instance, a correlation needs to be established between the
Jianjun Wang obtained his Ph.D. degree at University of Mainz (Germany) in 2006. From May 2007 to October 2009, he was a project leader at Max-Planck Institute for Polymer Research. Since April 2010, he has been a professor at ICCAS, and he has been a professor at the University of Chinese Academy of Sciences (UCAS) since March 2015. Dr. Wang’s current research interest focuses on molecular level understanding and controlling of ice formation, which are essential for broad applications such as anti-icing coatings, cryopreservation of cells and tissues, and templates for porous materials.
■
ACKNOWLEDGMENTS The authors are grateful for support from the Chinese National Nature Science Foundation (21733010, 51436004 and 21503240) and the Strategic Priority Research Program of the Chinese Academy of Sciences (CAS) (Grant XDA09020000). 1090
DOI: 10.1021/acs.accounts.7b00528 Acc. Chem. Res. 2018, 51, 1082−1091
Article
Accounts of Chemical Research
■
(24) Wilson, P. W.; Osterday, K. E.; Heneghan, A. F.; Haymet, A. D. J. Type I Antifreeze Proteins Enhance Ice Nucleation above Certain Concentrations. J. Biol. Chem. 2010, 285, 34741−34745. (25) Pandey, R.; Usui, K.; Livingstone, R. A.; Fischer, S. A.; Pfaendtner, J.; Backus, E. H. G.; Nagata, Y.; Fröhlich-Nowoisky, J.; Schmüser, L.; Mauri, S.; Scheel, J. F.; Knopf, D. A.; Pöschl, U.; Bonn, M.; Weidner, T. Ice-Nucleating Bacteria Control the Order and Dynamics of Interfacial Water. Sci. Adv. 2016, 2, e1501630. (26) Yang, H.; Ma, C.; Li, K.; Liu, K.; Loznik, M.; Teeuwen, R.; van Hest, J. C. M.; Zhou, X.; Herrmann, A.; Wang, J. Tuning Ice Nucleation with Supercharged Polypeptides. Adv. Mater. 2016, 28, 5008−5012. (27) He, Z.; Xie, W. J.; Liu, Z.; Liu, G.; Wang, Z.; Gao, Y. Q.; Wang, J. Tuning Ice Nucleation with Counterions on Polyelectrolyte Brush Surfaces. Sci. Adv. 2016, 2, e1600345. (28) Chen, X.; Yang, T.; Kataoka, S.; Cremer, P. S. Specific Ion Effects on Interfacial Water Structure near Macromolecules. J. Am. Chem. Soc. 2007, 129, 12272−12279. (29) Jungwirth, P.; Cremer, P. S. Beyond Hofmeister. Nat. Chem. 2014, 6, 261−263. (30) Geng, H.; Liu, X.; Shi, G.; Bai, G.; Ma, J.; Chen, J.; Wu, Z.; Song, Y.; Fang, H.; Wang, J. Graphene Oxide Restricts Growth and Recrystallization of Ice Crystals. Angew. Chem., Int. Ed. 2017, 56, 997−1001. (31) Geng, H.; Yao, B.; Zhou, J.; Liu, K.; Bai, G.; Li, W.; Song, Y.; Shi, G.; Doi, M.; Wang, J. Size Fractionation of Graphene Oxide Nanosheets Via Controlled Directional Freezing. J. Am. Chem. Soc. 2017, 139, 12517−12523. (32) Bai, G.; Song, Z.; Geng, H.; Gao, D.; Liu, K.; Wu, S.; Rao, W.; Guo, L.; Wang, J. Oxidized Quasi-Carbon Nitride Quantum Dots Inhibit Ice Growth. Adv. Mater. 2017, 29, 1606843. (33) Kuiper, M. J.; Lankin, C.; Gauthier, S. Y.; Walker, V. K.; Davies, P. L. Purification of Antifreeze Proteins by Adsorption to Ice. Biochem. Biophys. Res. Commun. 2003, 300, 645−648. (34) Knight, C. A.; Wen, D.; Laursen, R. A. Nonequilibrium Antifreeze Peptides and the Recrystallization of Ice. Cryobiology 1995, 32, 23−34. (35) Congdon, T.; Notman, R.; Gibson, M. I. Antifreeze (Glyco)Protein Mimetic Behavior of Poly(Vinyl Alcohol): Detailed Structure Ice Recrystallization Inhibition Activity Study. Biomacromolecules 2013, 14, 1578−1586. (36) Wu, S.; Zhu, C.; He, Z.; Xue, H.; Fan, Q.; Song, Y.; Francisco, J. S.; Zeng, X. C.; Wang, J. Ion-Specific Ice Recrystallization Provides a Facile Approach for the Fabrication of Porous Materials. Nat. Commun. 2017, 8, 15154. (37) Kreder, M. J.; Alvarenga, J.; Kim, P.; Aizenberg, J. Design of AntiIcing Surfaces: Smooth, Textured or Slippery? Nat. Rev. Mater. 2016, 1, 15003. (38) Lv, J.; Song, Y.; Jiang, L.; Wang, J. Bio-Inspired Strategies for AntiIcing. ACS Nano 2014, 8, 3152−3169. (39) Chen, J.; Luo, Z.; Fan, Q.; Lv, J.; Wang, J. Anti-Ice Coating Inspired by Ice Skating. Small 2014, 10, 4693−4699. (40) Dou, R.; Chen, J.; Zhang, Y.; Wang, X.; Cui, D.; Song, Y.; Jiang, L.; Wang, J. Anti-Icing Coating with an Aqueous Lubricating Layer. ACS Appl. Mater. Interfaces 2014, 6, 6998−7003. (41) Wang, J.-H. A Comprehensive Evaluation of the Effects and Mechanisms of Antifreeze Proteins During Low-Temperature Preservation. Cryobiology 2000, 41, 1−9. (42) Carpenter, J. F.; Hansen, T. N. Antifreeze Protein Modulates Cell Survival During Cryopreservation: Mediation through Influence on Ice Crystal Growth. Proc. Natl. Acad. Sci. U. S. A. 1992, 89, 8953−8957. (43) Vrbka, L.; Jungwirth, P. Brine Rejection from Freezing Salt Solutions: A Molecular Dynamics Study. Phys. Rev. Lett. 2005, 95, 148501. (44) Mahler, W.; Bechtold, M. F. Freeze-Formed Silica Fibres. Nature 1980, 285, 27−28. (45) Deville, S.; Saiz, E.; Nalla, R. K.; Tomsia, A. P. Freezing as a Path to Build Complex Composites. Science 2006, 311, 515−518. (46) Zhang, H.; Hussain, I.; Brust, M.; Butler, M. F.; Rannard, S. P.; Cooper, A. I. Aligned Two- and Three-Dimensional Structures by Directional Freezing of Polymers and Nanoparticles. Nat. Mater. 2005, 4, 787−793.
REFERENCES
(1) DeVries, A. L.; Wohlschlag, D. E. Freezing Resistance in Some Antarctic Fishes. Science 1969, 163, 1073−1075. (2) Graether, S. P.; Kuiper, M. J.; Gagne, S. M.; Walker, V. K.; Jia, Z.; Sykes, B. D.; Davies, P. L. [Beta]-Helix Structure and Ice-Binding Properties of a Hyperactive Antifreeze Protein from an Insect. Nature 2000, 406, 325−328. (3) Sun, T.; Lin, F.-H.; Campbell, R. L.; Allingham, J. S.; Davies, P. L. An Antifreeze Protein Folds with an Interior Network of More Than 400 Semi-Clathrate Waters. Science 2014, 343, 795−798. (4) Raymond, J. A.; DeVries, A. L. Adsorption Inhibition as a Mechanism of Freezing Resistance in Polar Fishes. Proc. Natl. Acad. Sci. U. S. A. 1977, 74, 2589−2593. (5) Knight, C. A. Structural Biology: Adding to the Antifreeze Agenda. Nature 2000, 406, 249−251. (6) Knight, C. A.; De Vries, A. L.; Oolman, L. D. Fish Antifreeze Protein and the Freezing and Recrystallization of Ice. Nature 1984, 308, 295−296. (7) Davies, P. L. Ice-Binding Proteins: A Remarkable Diversity of Structures for Stopping and Starting Ice Growth. Trends Biochem. Sci. 2014, 39, 548−555. (8) Graham, L. A.; Davies, P. L. Glycine-Rich Antifreeze Proteins from Snow Fleas. Science 2005, 310, 461. (9) Drori, R.; Li, C.; Hu, C.; Raiteri, P.; Rohl, A. L.; Ward, M. D.; Kahr, B. A Supramolecular Ice Growth Inhibitor. J. Am. Chem. Soc. 2016, 138, 13396−13401. (10) Deville, S.; Viazzi, C.; Leloup, J.; Lasalle, A.; Guizard, C.; Maire, E.; Adrien, J.; Gremillard, L. Ice Shaping Properties, Similar to That of Antifreeze Proteins, of a Zirconium Acetate Complex. PLoS One 2011, 6, e26474. (11) Deller, R. C.; Vatish, M.; Mitchell, D. A.; Gibson, M. I. Synthetic Polymers Enable Non-Vitreous Cellular Cryopreservation by Reducing Ice Crystal Growth During Thawing. Nat. Commun. 2014, 5, 3244. (12) Mizrahy, O.; Bar-Dolev, M.; Guy, S.; Braslavsky, I. Inhibition of Ice Growth and Recrystallization by Zirconium Acetate and Zirconium Acetate Hydroxide. PLoS One 2013, 8, e59540. (13) Liu, K.; Wang, C.; Ma, J.; Shi, G.; Yao, X.; Fang, H.; Song, Y.; Wang, J. Janus Effect of Antifreeze Proteins on Ice Nucleation. Proc. Natl. Acad. Sci. U. S. A. 2016, 113, 14739−14744. (14) Baardsnes, J.; Kondejewski, L. H.; Hodges, R. S.; Chao, H.; Kay, C.; Davies, P. L. New Ice-Binding Face for Type I Antifreeze Protein. FEBS Lett. 1999, 463, 87−91. (15) Garnham, C. P.; Campbell, R. L.; Davies, P. L. Anchored Clathrate Waters Bind Antifreeze Proteins to Ice. Proc. Natl. Acad. Sci. U. S. A. 2011, 108, 7363−7367. (16) Nutt, D. R.; Smith, J. C. Dual Function of the Hydration Layer around an Antifreeze Protein Revealed by Atomistic Molecular Dynamics Simulations. J. Am. Chem. Soc. 2008, 130, 13066−13073. (17) Liou, Y.-C.; Tocilj, A.; Davies, P. L.; Jia, Z. Mimicry of Ice Structure by Surface Hydroxyls and Water of a [Beta]-Helix Antifreeze Protein. Nature 2000, 406, 322−324. (18) Knight, C. A.; Cheng, C. C.; DeVries, A. L. Adsorption of AlphaHelical Antifreeze Peptides on Specific Ice Crystal Surface Planes. Biophys. J. 1991, 59, 409−418. (19) Scotter, A. J.; Marshall, C. B.; Graham, L. A.; Gilbert, J. A.; Garnham, C. P.; Davies, P. L. The Basis for Hyperactivity of Antifreeze Proteins. Cryobiology 2006, 53, 229−239. (20) Drori, R.; Davies, P. L.; Braslavsky, I. When Are Antifreeze Proteins in Solution Essential for Ice Growth Inhibition? Langmuir 2015, 31, 5805−5811. (21) Moore, E. B.; Molinero, V. Structural Transformation in Supercooled Water Controls the Crystallization Rate of Ice. Nature 2011, 479, 506−508. (22) Esser-Kahn, A. P.; Trang, V.; Francis, M. B. Incorporation of Antifreeze Proteins into Polymer Coatings Using Site-Selective Bioconjugation. J. Am. Chem. Soc. 2010, 132, 13264−13269. (23) Du, N.; Liu, X. Y.; Hew, C. L. Ice Nucleation Inhibition: Mechanism of Antifreeze by Antifreeze Protein. J. Biol. Chem. 2003, 278, 36000−36004. 1091
DOI: 10.1021/acs.accounts.7b00528 Acc. Chem. Res. 2018, 51, 1082−1091
