Skip to main content
NCBI home page
ACS AuthorChoice logoLink to ACS AuthorChoice
. 2020 Sep 14;12(40):45192–45201. doi: 10.1021/acsami.0c13295

Bioinspired Suprahelical Frameworks as Scaffolds for Artificial Photosynthesis

Kai Tao †,*, Bin Xue ‡,*, Shuyi Han ∥, Ruth Aizen §, Linda J W Shimon ⊥, Zhengyu Xu ‡, Yi Cao ‡, Deqing Mei †, Wei Wang ‡, Ehud Gazit §,*
PMCID: PMC7549093  PMID: 32924412

Abstract

graphic file with name am0c13295_0009.jpg

Framework materials have shown promising potential in various biological applications. However, the state-of-the-art components show low biocompatibility or mechanical instability, or cannot integrate both optics and electronics, thus severely limiting their extensive applications in biological systems. Herein, we demonstrate that amide-based bioorganic building blocks, including dipeptides and dipeptide nucleic acids, can self-assemble into hydrogen-bonded suprahelix architectures of controllable handedness, which then form suprahelical frameworks with diverse cavities. Especially, the cavities can be tuned to be hydrophilic or hydrophobic, and the shortest diagonal distance can be modulated from 0.5 to 1.8 nm, with the volume proportion in the unit cell changing from 5 to 60%. Furthermore, the hydrogen bonding networks result in high mechanical rigidity and semiconductively optoelectronic properties, which allow the utilization of the suprahelical frameworks as supramolecular scaffolds for artificial photosynthesis. Our findings reveal amide-based suprahelix architectures acting as bioinspired supramolecular frameworks, thus extending the constituents portfolio and increasing the feasibility of using framework materials for biological applications.

Keywords: amide-skeleton biomaterials, crystallization engineering, suprahelices, supramolecular frameworks, artificial photosynthesis

Introduction

Framework-based materials have attracted increasing interest in diverse well-established fields, such as catalysis, separation, sorption, and storage,1−5 as well as in the emerging ones including smart microchannels and selective screening-separation in biological systems.2,3,6 However, conventional inorganic constituents, such as zeolites, have intrinsically low biocompatibility and engineerability, thus severely restricting their uses, especially when interfacing complicated biological systems.7 Hybrid architectures such as metal–organic frameworks (MOFs) and hydrogen-bonded organic frameworks (HOFs) may ameliorate these shortcomings to some extent. However, their extensive applications are still limited due to several issues, including the involvement of metal ions, restricted biocompatibility, difficulty of morphological or functional modulation, and in many cases, complicated synthesis procedures and mechanical instability.3,8−13 Recently, several reports demonstrated that biological materials could form supramolecular frameworks by coordination with transition-metal ions (mainly zinc ions).14−16 Nevertheless, these architectures generally have multiple conformational energy landscape minima, resulting in high sensitivity to external factors (such as solvents and adsorbates) and mechanical instability.17,18 Therefore, there is a continuing demand for frameworks that can provide flexible modulation and improved properties, along with enhanced eco-friendliness and high structural rigidity.19−21

Herein, we demonstrate that amide-based bioinspired components, including dipeptides and dipeptide nucleic acids (diPNAs), can self-assemble into suprahelices, which further associate into supramolecular frameworks with controllable cavities. Furthermore, cavity parameters, including diagonal distances, helical pitches, and hydrophilic nature, can be easily tuned. Especially, the long-range and directional organization of the hydrogen bonds leads to bulky mechanical rigidity and semiconductively photoelectronic characteristics of the suprahelical frameworks, which are further demonstrated to be used as a basis for durable artificial photosynthesis scaffolds. Our findings establish suprahelical frameworks composed of simple bioorganic molecules, thus presenting a new bioinspired supramolecular alternative to complement the state-of-the-art counterparts.

Results and Discussion

Amide-Based Supramolecular Frameworks

Briefly, by combining hydrophobic amino acid side chains to amide backbones to promote aggregation (Table 1), several dipeptides composed of phenylalanine (F), valine (V), leucine (L), and isoleucine (I) were designed to crystallize into supramolecular architectures (Table S1 and Figure S3). Crystallographic characterizations demonstrated that only the FF,22VV, IV, and LV dipeptides formed cavity-containing frameworks (Table 1 and Figure S3).

Table 1. Molecular Structures and the Cavity Parameters of the Bioinspired Supramolecular Frameworks.

graphic file with name am0c13295_0007.jpg

graphic file with name am0c13295_0008.jpg

Open in a new tab

Scanning electron microscopy (SEM) characterizations demonstrated the large aspect-ratio, rod-like morphologies of the supramolecular architectures (Figures 1A–C and S4A). Crystallographic analyses revealed that the frameworks contained cavities of engineerable hydrophilicity and dimensions (Table 1, Figures 1E–G, and S4B). Specifically, FF molecules contributed the two benzyl side chains on the same side of the amide backbone and formed one-dimensional (1-D) hydrophilic channels composed of six monomeric backbones (Figure 1E),22 showing a shortest diagonal distance of 1.23 nm with a cavity volume of 462.87 Å3 and 16.8% occupation of the unit cell (Table 1). The channels were axially immobilized (along the c direction) through 2.88 Å parallel β-sheet hydrogen bonds (Namide···Ocarboxylic) between the amide backbones (Figure S5, “1”) and connected with each other (along the ab plane) by edge-to-face aromatic interactions with dihedral angles of 60–85° (Figure S5, “2”), thus generating an array of hydrophilic channels (Figure 1I). By contrast, in the VV system, the two isopropyl side chains were distributed on the opposite sides of the amide backbone and composed hydrophobic 1-D channels (Figure 1F), showing a shortest diagonal distance of 0.83 nm with a cavity volume of 271.19 Å3 and 14.4% occupation of the unit cell (Table 1). The channels were connected with each other (along the ab plane) through three hydrogen bonds of 2.71 Å (Namino···Ocarboxylic), 2.98 Å (Namide···Ocarboxylic), and 2.79 Å (Namino···Oamide) (Figure S6), thus forming an array of hydrophobic channels (Figure 1J).

Figure 1.

Figure 1

Open in a new tab

Morphology and cavity characterizations of the bioinspired supramolecular frameworks. (A, E, I) FF; (B, F, J) VV; (C, G, K) LV; (D, H, L) diPNA-GC. (A–D) Scanning electron microscopy images of the supramolecular frameworks. (E–H) Crystallographic images showing the molecular organizations comprising the cavities of the frameworks. The magenta quadrangles indicate the suprahelix structures. The colored graphics denote the cavities (channels or voids) inside the frameworks, with the hydrophilic and hydrophobic cavities designated in red and green, respectively. In (H), two views, (top) along the c direction and (bottom) along the a direction of the channels inside the diPNA-GC frameworks, are shown. (I–L) Schematic graphics showing the cavity arrays inside the frameworks. The hexahedrons represent the unit cell axes of the crystals.

Intriguingly, the IV dipeptide formed supramolecular frameworks similar to VV (Figure S4), producing arrays of hydrophobic channels with a shortest diagonal distance of 0.74 nm and a cavity volume of 217.06 Å3 with 11.1% occupation of the unit cell (Table 1). Simultaneously, the channels were connected through hydrogen bonds of 2.73 Å (Namino···Ocarboxylic), 2.97 Å (Namide···Odecarboxylic), and 2.80 Å (Namino···Oamide) (Figure S7, “1”). These findings demonstrate that the replacement of the side-chain isopropyl group to a sec-butyl group did not disturb the subtle force equilibrium and allowed to retain the channel conformations, indicating that to some extent, the frameworks could counterbalance the variation of steric hindrance. In contrast, when substituting the sec-butyl group with an isobutyl one, as in the LV dipeptide, the minor shift of the methyl group to the cavity center in the side chain resulted in significant spatial hindrance and decreased the size of the cavity. To offset this energy perturbation, the cavity conformation significantly transformed. As shown in Figure 1G, in the LV system, the 1-D channels disappeared and a six-petal Hong Kong orchid tree-like void was formed instead, with a shortest diagonal distance of 0.45 nm and a cavity volume of 459.93 Å3 with 5.4% occupation of the unit cell (Table 1), significantly smaller than those of the VV or IV cavities. Particularly, the central large void was further surrounded by six relatively narrower ones, each formed by two alternating circles (Figure S8). This resulted in a bulky distribution of discrete voids in the frameworks (Figure 1K). The two circles were both mediated by hydrogen bonds among the six LV monomers. In one circle, the six side-chain isopropyl groups pointed inside by forming two groups of hydrogen bonds of 2.77, 2.74 and 2.72 Å at the terminal carboxyl and amino groups between adjacent monomers, herein termed the “V circle” (Figure S8, “1”). By contrast, in the other circle, the six isobutyl moieties were directed inside with four water molecules participating in the circulation by forming two pairs of hydrogen bonds of 2.78 Å (Namino···Ocarboxylic), 2.66 Å (Namino···Owater), 2.67 Å (Owater···Owater), 2.74 Å (Owater···Ocarboxylic), and 2.75 Å (Namino···Ocarboxylic), thus designated the “L circle” (Figure S8, “2”). The two circles were tightly linked through extensive hydrogen bonding networks (Figure S9), thus counterbalancing the steric hindrance derived from the methyl group shifting and stabilizing the frameworks.

Considering the role of hydrogen bonding in the formation of amide-based supramolecular architectures,23,24 the close contacts of the relevant elements (oxygen and nitrogen atoms) were further investigated via Hirshfeld surface analysis (Figure S10).25Figure 2 demonstrates that oxygen atoms mostly contributed to the hydrogen bond formation in the dipeptides-based suprahelical frameworks, with the hydrogen bonds formed by nitrogen atoms found to be negligible. Also, the two-dimensional (2-D) fingerprint plots were nearly mirrored along the de = di division line (Figure S10), resulting in similar Oinside–Alloutside and Allinside–Ooutside ratios, thus indicating the reciprocal Oinside–Alloutside (Allinside–Ooutside) contacts.

Figure 2.

Figure 2

Open in a new tab

Statistics of the close contact of elements of the suprahelical frameworks from the 2-D fingerprint plots of the Hirshfeld surface. The red and blue bars indicate oxygen and nitrogen atoms, respectively.

We aimed to introduce additional hydrogen bonding interactions, especially at the side chains, to develop supramolecular frameworks with larger cavities. Therefore, a PNA with complementary nucleobases as the side chains was synthesized using an Fmoc solid-phase synthesis strategy (see Materials and Experimental Section) to self-assemble into supramolecular structures.26 Given the robust propensity of nucleobases to form Watson–Crick hydrogen bonding interactions, PNA-based building blocks have been reported to organize into supramolecular architectures significantly distinct from those formed by the peptide-based counterparts.27−29 We previously reported that diPNA-Guanine-Cytosine (diPNA-GC) could self-assemble into 1-D optoelectronic architectures.29 Crystallographic characterization demonstrated that Watson–Crick base pairing interactions were formed between the side-chain G and C moieties, with three hydrogen bonds of 2.82 Å (NC–OG), 2.91 Å (NG–NC), and 2.85 Å (NG–OC) (Figure S11, “2”). Combined with the parallel-displaced aromatic interactions of 3.46 and 3.49 Å along the axial direction (c direction, Figure S11, “1”),29 the synergy of these interactions resulted in the amide backbones distributed outwards (Figure S11, “3”), thus constructing multichannel frameworks (Figure 1H), with a shortest diagonal distance of 1.78 nm along the c direction and 0.90 nm along the a direction (Table 1). This resulted in a significantly high cavity volume of up to 3660.74 A3 and 59.4% occupation of the unit cell (Table 1). The 2-D fingerprint plots from the Hirshfeld surface analysis demonstrate that new contacts (peaks) emerged in the diPNA-GC crystals compared to the dipeptide-based counterparts (Figure S12). Especially, the nitrogen elements significantly contributed to the hydrogen bonding interactions, with a total 10.0% ratio, along with 35.7% for oxygen atoms (Figure 2). These results confirmed the interactions between individual diPNA-GC molecules had been strengthened compared to the dipeptide counterparts,30 thus demonstrating that the introduction of hydrogen bonding at the side chains can indeed develop frameworks with larger cavities.

Suprahelix Underlying the Supramolecular Frameworks

Intriguingly, the cavities inside the supramolecular frameworks were composed of hydrogen-bonded helical structures, as shown in Figure 3. However, the helix configurations, including the handedness, pitch length, and number of monomers per pitch, varied among the different frameworks (Figure 3and Table 2). Especially, the supramolecular helices were formed through head (amino)-to-tail (carboxylic) hydrogen bonding of six monomers in the peptide systems, in contrast to Watson–Crick hydrogen bonding through four side-chain nucleobases in the diPNA assemblies (Figure 3). Specifically, in the FF system, six peptide molecules interacted through the carboxylic and amino groups with a 2.75 Å hydrogen bond (Namino···Ocarboxylic) (Figure 3A, blue dotted lines), thus forming a left-handed supramolecular helix with a pitch of 3.28 nm (Table 2).23,31 In addition, each FF monomer connected with a water molecule (Figure 3A, marked with “①”) with a hydrogen bond of 2.86 Å (Namino···Owater) (Figure 3A, magenta dotted lines). Another water molecule (Figure 3A, marked with “②”) served to bridge the water ① molecules, thus forming a helix of water molecules inside the channel with two types of hydrogen bonds, 2.82 Å (O①–O②) and 3.08 Å (O②–O①) (Figure 3A, green dotted lines).32 This structure is consistent with the hydrophilic nature of the FF channels. In contrast, the helix compositions of the hydrophobic channels were relatively simpler, showing only head-to-tail, right-handed hydrogen bonds (Table 2). The VV and IV-based suprahelices were organized by 2.82 and 2.83 Å hydrogen bonds (Namino···Ocarboxylic), respectively (Figures 3B and S7, “1”), forming the same pitch of 1.03 nm (Table 2), while the LV suprahelices were organized by a 2.68 Å hydrogen bond (Namino···Ocarboxylic) (Figure 3C) with a pitch of 2.34 nm (Table 2). Nevertheless, in contrast to the peptides, the diPNA-GC-based suprahelix showed right-handedness with a large pitch of 3.34 nm albeit the presence of only four monomers per pitch (Table 2 and Figure 3D), since both the backbone and side chains contributed to suprahelix formation.

Figure 3.

Figure 3

Open in a new tab

Illustrative depiction of the helix conformations underlying the suprahelical frameworks. (A–C) A pitch of (A) FF left-handed, (B) VV, and (C) LV right-handed suprahelices from a (top) front and (bottom) lateral view. (D) A pitch of diPNA-GC right-handed suprahelix viewed from two different directions. The carbon, oxygen, and nitrogen atoms are designated in gray, red, and blue, respectively; the hydrogen atoms and side chains are neglected for clarity. The dotted lines represent the hydrogen bonds; the colors distinguish different groups, with the bond length values labeled in the corresponding colors. In (A), the two types of water molecules participating in crystallization and playing different roles are numerically marked.

Table 2. Summary of the Helical Parameters of the Bioinspired Suprahelical Frameworks.

building block handedness pitch (nm) no. of monomers/pitch
FF left 3.28 6
VV right 1.03 6
IV right 1.03 6
LV right 2.34 6
diPNA-GC right 3.34 4
Open in a new tab

Mechanical Rigidity of the Suprahelical Frameworks

A long-range hydrogen bonding network can result in high mechanical rigidity.32−35 For example, the well-studied β-sheet-based proteinaceous nanofibers self-assembled by the amyloid-β polypeptides, as well as ultrashort peptide crystals, can show Young’s moduli of 1–30 GPa (Figure 4A, magenta dashed-line region).35−39 However, several studies reported that helix-containing peptide assemblies, such as coiled-coil architectures, present significantly higher mechanical rigidity.40−42 Therefore, we examined the mechanical properties of the suprahelical frameworks using atomic force microscopy nanoindentation. The statistical analysis revealed these supramolecular architectures to display Young’s moduli of 6–40 GPa (Figure 4A, red dashed-line region, Figure S13). Correspondingly, their point stiffness values were in the range of 90–190 N m–1 (Figures 4B and S14). Specifically, the diPNA-GC assemblies showed the highest value, with a measured Young’s modulus of up to 37.4 ± 7.5 GPa and point stiffness of 183.5 ± 56.9 N m–1, thus confirming that the helix-based conformations are more expedient for mechanical applications than the state-of-the-art β-sheet-based counterparts.42 Notably, the mechanical rigidity of the suprahelical frameworks is between those of inorganic zeolite (usually higher than 30 GPa)43 and hybrid MOFs (usually lower than 30 GPa)44−46 (Figure 4A), thus supplying a new type of bioinspired alternative to bridge the gap. Nevertheless, it should be noted that the temperature can affect the bioinspired frameworks.47,48 For example, when heating to 250 °C, the FF crystals converted into to cyclic-FF ones, as confirmed by X-ray diffraction (XRD) and SEM characterizations (Figure S15). Therefore, to be suitable for high-temperature applications, the thermal stability of the suprahelical frameworks should be further enhanced, for instance by increasing the hydrogen bonding interactions.49

Figure 4.

Figure 4

Open in a new tab

Mechanical properties of the bioinspired suprahelical frameworks. (A) Comparison of Young’s moduli of peptide-based supramolecular materials and state-of-the-art porous counterparts. The magenta and red dashed-line frameworks label the regions of the characteristic β-sheet-based peptide self-assembled materials and the suprahelical frameworks, respectively. Young’s modulus data: Inorganic zeolites, ref (43); MOFs, ref (44); Aβ(1–40) fibers, ref (39); Cyclo-FW crystals, ref (32); dragline silk and insulin, ref (33); tobacco mosaic virus (TMV) nanotubes, ref (38). (B) Point stiffness statistics for the examined suprahelical frameworks, as indicated.

Suprahelical Frameworks as Bioinspired Scaffolds for Artificial Photosynthesis

The cavity nature and high mechanical rigidity suggest the suprahelical frameworks as candidate supramolecular scaffolds for biocatalytic applications.50 A Brunauer–Emmett–Teller (BET) measurement demonstrated the apparent average pore diameter to be 2.5–3.5 nm (Table S2) for the various assemblies, consistent with the crystallographic data presented above, with the pore volume ranging from 0.008 to 0.14 cm3 g–1. Correspondingly, the specific surface area was measured to be 12.40 m2 g–1 for IV to 68.1 m2 g–1 for diPNA-GC (Table S2). The results demonstrate the relatively small porous characteristic of the supramolecular scaffolds.21,22 We further focused on the diPNA-GC-based framework due to its higher porous fraction and mechanical rigidness (Figure S16). The extensive hydrogen bonding network can reduce the band gap of peptide assemblies, thus resulting in semiconductively optoelectronic features.23,51 Therefore, the band structures were first calculated for computationally optimized diPNA-GC crystal frameworks (Figure 5A). Compared to 3.63 eV for the single molecule (Figure 5A-i), the band gap for the crystallized structure was 3.46 eV (Figure 5A-ii), thus confirming that the hydrogen bonding organization indeed decreased the electron transfer energy barriers and establishing the diPNA-GC assemblies as supramolecular, wide-gap semiconductors.32,51 Furthermore, we plotted the crystal band structure along a from Γ to π/a and along c from Γ to π/c. The highest occupied molecular orbital of the diPNA-GC molecule in the crystal was split into four energy levels at the Γ point (Figure 5A-iii). Interestingly, the four energy levels could be further divided into two groups with an energy separation of 0.18 eV, each group composed of two bands and the upper levels separated by 0.067 eV (Figure 5A-ii), as a result of the G-C Watson–Crick interactions. Similarly, the lowest unoccupied molecular orbital in the crystalline structure was also split into several energy bands, with band dispersions within 0.05 eV along both the c and a direction (Figure 5A-iv). Therefore, the intrinsic wide-gap semiconductivity nature and the delicate band splitting with ultrasmall energy differences led to the wide-spectrum photon-electron transformation of the diPNA-GC frameworks, as further confirmed by fluorescent microscopy characterizations (Figure S17).

Figure 5.

Figure 5

Open in a new tab

Artificial photosynthesis using the diPNA-GC-based suprahelical frameworks as the scaffolds. (A) Band structures (calculated with the HSE06 functional) for (i) diPNA-GC single molecule, (ii) diPNA-GC crystal near the Fermi level, (iii) diPNA-GC crystal valence bands near the Fermi level, and (iv) diPNA-GC crystal conduction band near the Fermi level. The band gap values are labeled at the corresponding places. (B) Schematic representation of the artificial photosynthesis configuration. (C) Cyclic voltammogram of Ru(bpy)3Cl2. (D) Photocurrent response and (E) time-resolved photoinduced UV absorption at 265 nm of nicotinamide adenine dinucleotide (NAD+) in the presence of the diPNA-GC frameworks. (F) Conversion percentage of reduced nicotinamide adenine dinucleotide (NADH) in the presence of the artificial photosynthesis system shown in (B). In (C, D, F), the same experiments without the suprahelical frameworks are shown as controls.

To examine whether the diPNA-GC frameworks could facilitate photoelectron production and transfer,52,53 an artificial photosynthesis prototype was developed using the diPNA-GC-based frameworks as the skeleton structures (Figure 5B). Cyclic voltammetry characterization demonstrated that the suprahelical architectures showed a notable catalytic property for electro-redox of tris(2,2′-bipyridyl)dichlororuthenium(II) hexahydrate (Ru(bpy)3Cl2·6H2O), which generally acts as the electron mediator in photosynthesis systems,54 with a reduction potential peak of −0.39 V, compared to −0.58 V for the control (Figure 5C), illustrating the significant electron transfer ability of the frameworks. Furthermore, photocurrent measurements using triethanolamine (TEOA) as an electron donor illustrated that an indium tin oxide (ITO) glass slide coated with a ruthenium-complex-containing diPNA-GC crystal powder could produce a remarkably high photocurrent upon irradiation by a 350 W Xe lamp (Figure 5D), showing a value 6.5-fold higher (6.5 μA) than that produced by the control ruthenium-complex-coated ITO slide (1.0 μA). This result demonstrates that the suprahelical frameworks can facilitate the delocalization of excitons and suppress electron–hole recombination during photoelectrons production, consistent with the electron level analysis. The UV–vis absorption characterization demonstrated that the concentration of NAD+ significantly decreased over time in the presence of diPNA-GC crystals mixed with Ru(bpy)3Cl2 under illumination (Figure 5E), thus indicating the feasibility of utilizing the suprahelical framework-supported photosensitizers as the sunlight-sensitive antennas to produce NADH, which is required in many biocatalytic redox reactions.50,54 Finally, after sputtered with Pt nanoparticles (NPs) as the catalytic centers, the hybrid system (diPNA-GC/Ru/Pt) presented a remarkable catalytic activity of NADH regeneration, showing a yield of ∼21% after 2 h, approximately 7-fold higher than the Ru/Pt control (Figure 5F). As additional controls, artificial photosynthesis systems were constructed employing other suprahelical frameworks with lower cavity ratios as the scaffolds, showing reduced efficiency compared to diPNA-GC (Figure S18). Furthermore, the mechanical rigidity promoted easy retrieval of the diPNA-GC frameworks for storage and reusability, with approximately 50% NADH conversion yield after five cycles without obvious detachment from the substrate (Figure S19). Especially, XRD and SEM characterizations demonstrated that after recycling, the frameworks still kept intact (Figure S16), thus implying the stability of the crystals and potentially allowing to reduce costs and contaminations.

Conclusions

In summary, we demonstrate that amide-based bioinspired building blocks, including dipeptides and diPNAs, can self-assemble into hydrogen-bonded suprahelices, which finally form suprahelical frameworks. Especially, the extensive and directional hydrogen bonds endowed the frameworks high mechanical rigidity, thus bridging the gap between rigid but nonbiocompatible zeolites and instable hybrid MOFs or HOFs. The intrinsic semiconductively optoelectronic properties endow the suprahelical frameworks the ability to be used as durable skeletons to support photosensitizers and catalysts, along with prompting photoelectron production and transfer for artificial photosynthesis.

Considering the diversity of the amino acid side chains and the nucleotide bases, as well as the intrinsic chirality and the feasibility of chemical or physical modifications of the monomers, the amide-based assembly strategy can be engineered to design suprahelices with unique properties, thus extending the constituents repertoire of cavity-containing materials. Moreover, the bioinspired suprahelical frameworks can be explored for additional applications, such as biomimetic, smart microchannels, and selective screening-separation, thus expanding the applications of bioorganic supramolecular frameworks. Our work demonstrates, for the first time, the structural basis underlying amide-based supramolecular frameworks, thus supplying an alternative conceptual design for preparing and modulating bioinspired frameworks.

Materials and Experimental Section

Materials

The dipeptides were purchased from Bachem (Bubendorf, Switzerland), GL Biochem (Shanghai, China), or DgPeptides (Hangzhou, China). N-terminal and side-chain-protected PNA monomers (Fmoc-PNA-G(Bhoc)-OH, Fmoc-PNA-C(Bhoc)-OH) were purchased from Polyorg (Leominster, MA), O-(1H-benzotriazole-1-yl)-N,N,N′,N′-tetramethyluronium hexafluorophosphate (HBTU) and N-hydroxybenzotriazole anhydrous (HOBt) from Chem-Impex International (Wood Dale, IL), N,N′-diisopropylethylamine (DIEA) and triisopropylsilane (TIS) from Sigma-Aldrich (Rehovot, Israel), Rink Amide MBHA resin from Merck (Darmstadt, Germany), trifluoroacetic acid (TFA), dichloromethane (DCM), and N,N-dimethylformamide (DMF) of peptide synthesis purity grade from Bio-Lab (Jerusalem, Israel), tris(2,2′-bipyridyl)dichlororuthenium(II) hexahydrate (Ru(bpy)3Cl2·6H2O) and nicotinamide adenine dinucleotide (NAD+) from Aladdin (Shanghai, China), and triethanolamine (TEOA) from Sinopharm (Shanghai, China). All materials were used as received without further purification. Water was processed by a Millipore purification system (Darmstadt, Germany) with a minimum resistivity of 18.2 MΩ cm.

DiPNA-GC Synthesis

The diPNA-GC was synthesized using the standard Fmoc solid-phase synthesis method.29 After deprotection of the MBHA resin with 20% piperidine and 0.1 M HOBt in DMF, Fmoc-PNA-C(Bhoc)-OH was introduced for coupling, followed by introduction of Fmoc-PNA-G(Bhoc)-OH. The carboxylic groups were activated by treatment with HBTU/HOBt/DIEA, transforming the carboxylic acids into activated esters to react with the deprotected α-amine groups. After synthesis, cleavage from the resin and deprotection of the side chains were co-performed using a mixture of TFA, TIS, and H2O at a ratio of 95:2.5:2.5. The cleavage mixture and subsequent DCM washing solution were then purged with nitrogen. The obtained concentrated solutions were added to water and lyophilized. The product identity was verified by electrospray ionization time-of-flight mass spectrometry and reversed-phase high-performance liquid chromatography (Figures S1 and S2).

Crystals Preparation

The dipeptides or the synthesized diPNA-GC powders were added to water or commercial 1.0 M BICINE buffer at pH 9.0 (Hampton Research, CA). The solutions were heated in a water bath at 80 °C for 5 min to ensure the complete dissolution of the solutes, followed by filtration using a 0.45 μm PVDF membrane (Merck Millipore, Carrigtwohil, Ireland). The filtered solutions were placed at room temperature and needle-like crystals appeared at the bottom of the vials after several hours and reached maximal size after 30 days. The supernatants were removed and the crystals were washed with water three times and collected for later use.

Scanning Electron Microscopy (SEM)

The solution containing the crystals was placed on a clean glass slide, allowed to adsorb for a few seconds and excess liquid was removed with filter paper. The slide was then coated with Cr and observed under a JSM-6700 field emission scanning electron microscope (JEOL, Tokyo, Japan) operated at 10 kV.

X-ray Crystallography

A single crystal suitable for X-ray diffraction was coated with Paratone oil (Hampton Research, CA), mounted on a MiTeGen loop and flash frozen in liquid nitrogen. Diffraction data were measured with Cu Kα radiation at 100(2) K using a Rigaku XtaLabPro with a Dectris PilatusR 200K-A detector. The data were processed using CrysAlisPro 1.171.39.22a. The structures were determined by direct methods using SHELXT-2013 and SHELXT-2016/4 and refined by full-matrix least squares against F2 with SHELXL-2013 and SHELXL-2016/4. All nonhydrogen atoms were refined aniostropically. Hydrogen atoms were placed in calculated positions and refined in riding mode. The SQUEEZE protocol of Platon was implemented for the LI structure due to disordered solvent cavities. The crystal data (cif. files) have been deposited with the CSD (Table S1).

Young’s Modulus Measurement

Atomic force microscopy (AFM) experiments were carried out using a commercial AFM (JPK, Nanowizard II, Berlin, Germany). The force curves were obtained using the commercial software from JPK and analyzed by a custom-written procedure based on Igor pro 6.12 (Wavemetrics, Inc.). Silica cantilevers (RTESPA-525 Bruker Company with the half-open angle of the pyramidal face of θ < 10°, tip radius: ∼8 nm, frequency in air: ∼525 kHz) were used in all experiments. The spring constant of the cantilevers was ∼200 N m–1. The maximum loading force was set at 800 nN. All AFM experiments were carried out at room temperature. In a typical experiment, the crystal samples were cast on the surface of the glass substrate and the cantilever was moved over the crystal at a constant speed of 15 μm s–1 guided by an optical microscope. The cantilever was held on the crystal surface at a constant force of 800 nN. Then, the cantilever was retracted and moved to another spot for the next cycle. The indentation fit was performed using an Igor custom-written program and manually checked after the fitting was complete. The curves were then fitted manually. Each approaching force–deformation curve was fitted in the range of 10 nm from the contact point, or from the maximum indentation depth to the contact point if the former was less than 10 nm. By fitting the approaching curve to the Hertz model (1), we could obtain the Young’s modulus of the crystals. Typically, three to four such regions (5 μm × 5 μm, 400 pixels) were randomly selected on each crystal to construct the elasticity histogram.

graphic file with name am0c13295_m001.jpg 1

where F is the stress of the cantilever, h is the depth of the crystal pressed by the cantilever tip, α is the half-angle of the tip, E is the Young’s modulus of the crystal, and ν is the Poisson ratio. We chose ν = 0.3 in our calculations.

Point Stiffness Calculations

The measured point stiffness (kmeas) is composed of the stiffness constants of the cantilever (kcan) and the crystals (kcry). Assuming that the crystal and the cantilever act as two springs oriented in a series, the point stiffness of the crystal could be calculated using the following relation: Using eq 2 and an average measured value for kmeas, the average stiffness of the crystal could be calculated. To estimate the material property of the crystals, it was assumed that the mechanical behavior of the crystal could be described as linear elastic, which is a good approximation for solids under small strains.

graphic file with name am0c13295_m002.jpg 2

Brunauer–Emmett–Teller (BET) Surface Area Analysis

The N2 adsorption isotherm was undertaken at 77 K using a Micromeritics 3Flex instrument.

Computational Optimization of the diPNA-GC Crystal Structure

Calculations were carried out using the Vienna Ab initio Simulation Package VASP 5.3 within the framework of density functional theory (DFT).55,56 The projector augmented-wave (PAW) method was applied to treat both core and valence electrons.56 The Kohn–Sham equations57,58 were solved using a plane-wave basis set, with an energy cutoff of 600 eV. The Perdew–Burke–Ernzerhof (PBE) generalized gradient approximation (GGA) exchange-correlation functional59 was used. However, to correct for underestimation in band gap prediction when using PBE, calculations using the range-separated hybrid Heyd–Scuseria–Ernzerhof (HSE) functional,60 with a range-separation μ of 0.11 Bohr–1 (HSE06),61 were carried out. The GGA optPBE functional62 was used to account for London dispersion. All atomic geometries were fully relaxed until forces were less than 0.01 eV Å–1. 2 × 2 × 2 κ-point sampling was used for the triclinic cell and a Gaussian smearing width of 0.05 eV was used for κ space integrals.

UV–Vis Absorption Spectroscopy

UV–vis spectra were measured using a V-550 (JASCO Inc. Japan) spectrophotometer. The cuvette width was 1 cm, and the bandwidth was set at 0.2 nm.

Preparation of the Suprahelical Frameworks/Ruthenium-Complex-Coated Indium Tin Oxide (ITO)

The crystals dispersed in water (5.0 mg mL–1) were dropped on the ITO and dried under N2 for 8 h. Ruthenium solution (1.0 mg mL–1) was then dropped on the crystal-coated ITO and dried under N2 for another 8 h.

Photocurrent Measurement

The suprahelical frameworks and ruthenium-complex-coated ITO glass slide were incubated in phosphate buffer (100.0 mM, pH 6.0) containing 15% (w/v) TEOA as an electron donor and periodically illuminated with visible light from a 350 W Xe lamp. The photocurrent was measured using an electrochemical workstation under a working voltage of 1.2 V. The ITO glass slide coated with ruthenium complex alone was used as a control.

Cyclic Voltammogram (CV)

The suprahelical framework-coated glassy carbon electrode was placed in an electrolytic cell containing 1.0 mg mL–1 Ru(bpy)3Cl2. A 3-electrode system was used to obtain cyclic voltammogram: the crystal-modified glassy carbon (working electrode), Ag/AgCl (reference electrode), and a platinum wire (counter electrode). The cyclic voltammetry curves of Ru(bpy)3Cl2 were obtained using a scanning rate of 100.0 mV s–1 and constant illumination of visible light from a Xe lamp.

Visible Light-Driven NADH Regeneration

First, a film of platinum nanoparticles (Pt NPs), approximately 25 nm thick, was coated on the ITO by evaporation. Photochemical regeneration of NADH was performed in a quartz reactor at room temperature. 1.0 mM NAD+ was dissolved in phosphate buffer (100.0 mM, pH 6.0) containing 15% (w/v) TEOA. The Pt NPs-sputtered suprahelical frameworks-coated glass slide was then dispersed in the reaction solution and exposed to visible light from a Xe lamp. The concentration of regenerated NADH was calculated based on the absorbance at 340 nm using a spectrophotometer (JASCO, Tokyo, Japan). As a control, only ruthenium complex and Pt NPs were coated on the ITO and the regeneration of NADH was performed and measured as described above. For sustainability study, the diPNA-GC-based photosynthesis system was removed from the solution, rinsed clean with water, and then immersed in another reaction cell.

Powder X-ray Diffraction (PXRD)

The PXRD patterns were recorded with a Bruker D8 diffractometer using Cu Kα1 (λ = 1.5405 Å) radiation with a step of 0.02 at a scanning speed of 8 s per step.

Hirshfeld Surface Analysis

Fingerprint plots of Hirshfeld surfaces were drawn using the CrystalExplorer software.63

Acknowledgments

This work was supported in part by the European Research Council under the European Union Horizon 2020 research and innovation program (no. 694426) (E.G.), Joint NSFC-ISF Grant (no. 3145/19) (E.G.), National Natural Science Foundation of China (no.11804148) (B.X.), Natural Science Foundation of Jiangsu province (no. BK20180320) (B.X.), and the Fundamental Research Funds for the Central Universities (no. 020414380118) (B.X.). The authors thank Dr. Ruth Pachter and Dr. Jie Jiang for the band gap calculation assistance, Dr. Sigal Rencus-Lazar for language editing, and the members of Gazit and Cao laboratories for helpful discussions.

Supporting Information Available

The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acsami.0c13295.

  • MS spectrum of the synthesized diPNA-GC (Figure S1); reversed-phase high-performance liquid chromatography (HPLC) profile of the synthesized diPNA-GC (Figure S2); crystallographic structures of the dipeptides and diPNA crystals (Figure S3); morphological and cavity characterization of the supramolecular frameworks assembled by IV (Figure S4); crystallographic packing of FF self-assembling frameworks (Figure S5); molecular structures of VV assembling frameworks (Figure S6); molecular structures of IV assembling frameworks (Figure S7); crystallographic structures of the LV supramolecular frameworks (Figure S8); magnified representation of the hydrogen bonding network (Figure S9); Hirshfeld surface and the 2-D fingerprint plot (Figures S10 and S12); packing structures of the diPNA-GC supramolecular frameworks (Figure S11); statistical Young’s modulus distribution of the bioinspired suprahelical frameworks (Figure S13); statistical point stiffness distribution of the bioinspired suprahelical frameworks (Figure S14); SEM images and XRD spectra (Figure S15); XRD characterizations of the original diPNA-GC frameworks (Figure S16); fluorescence microscopy images of the diPNA-GC self-assembling suprahelical frameworks (Figure S17); comparison of the artificial photosynthesis systems using the amide-based suprahelical frameworks as scaffolds (Figure S18); dipeptide/diPNA sequences examined in this work and their crystal structure parameters (Table S1); and apparent porous parameters of the bioinspired suprahelical frameworks (Table S2) (PDF)

Author Contributions

K.T. and B.X. contributed equally. The manuscript was written through contributions of all authors. All authors have given approval to the final version of the manuscript.

The authors declare no competing financial interest.

Supplementary Material

am0c13295_si_001.pdf (2.7MB, pdf)

References

  1. Diercks C. S.; Yaghi O. M. The Atom, the Molecule, and the Covalent Organic Framework. Science 2017, 355, eaal1585 10.1126/science.aal1585. [DOI] [PubMed] [Google Scholar]
  2. Davis M. E. Ordered Porous Materials for Emerging Applications. Nature 2002, 417, 813–821. 10.1038/nature00785. [DOI] [PubMed] [Google Scholar]
  3. Furukawa H.; Cordova K. E.; O’Keeffe M.; Yaghi O. M. The Chemistry and Applications of Metal-Organic Frameworks. Science 2013, 341, 1230444 10.1126/science.1230444. [DOI] [PubMed] [Google Scholar]
  4. Horike S.; Shimomura S.; Kitagawa S. Soft Porous Crystals. Nat. Chem. 2009, 1, 695–704. 10.1038/nchem.444. [DOI] [PubMed] [Google Scholar]
  5. Li J.-R.; Kuppler R. J.; Zhou H.-C. Selective Gas Adsorption and Separation in Metal-Frameworks. Chem. Soc. Rev. 2009, 38, 1477–1504. 10.1039/b802426j. [DOI] [PubMed] [Google Scholar]
  6. Lin R. B.; He Y.; Li P.; Wang H.; Zhou W.; Chen B. L. Multifunctional Porous Hydrogen-Bonded Organic Framework Materials. Chem. Soc. Rev. 2019, 48, 1362–1389. 10.1039/C8CS00155C. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Ma Y.; Tong W.; Zhou H.; Suib S. L. A Review of Zeolite-Like Porous Materials. Microporous Mesoporous Mater. 2000, 37, 243–252. 10.1016/S1387-1811(99)00199-7. [DOI] [Google Scholar]
  8. Zhou H.-C.; Long J. R.; Yaghi O. M. Introduction to Metal-Organic Frameworks. Chem. Rev. 2012, 112, 673–674. 10.1021/cr300014x. [DOI] [PubMed] [Google Scholar]
  9. Shen K.; Zhang L.; Chen X.; Liu L.; Zhang D.; Han Y.; Chen J.; Long J.; Luque R.; Li Y.; Chen B. L. Ordered Macro-Microporous Metal-Organic Framework Single Crystals. Science 2018, 359, 206–210. 10.1126/science.aao3403. [DOI] [PubMed] [Google Scholar]
  10. Snurr R. Q. It’s an Interesting MOF, but Is It Stable?. Matter 2019, 1, 26–27. 10.1016/j.matt.2019.06.014. [DOI] [Google Scholar]
  11. He Y.; Xiang S.; Chen B. L. A Microporous Hydrogen-Bonded Organic Framework for Highly Selective C2H2/C2H4 Separation at Ambient Temperature. J. Am. Chem. Soc. 2011, 133, 14570–14573. 10.1021/ja2066016. [DOI] [PubMed] [Google Scholar]
  12. Luo X. Z.; Jia X. J.; Deng J. H.; Zhong J. L.; Liu H. J.; Wang K. J.; Zhong D. C. A Microporous Hydrogen-Bonded Organic Framework: Exceptional Stability and Highly Selective Adsorption of Gas and Liquid. J. Am. Chem. Soc. 2013, 135, 11684–11687. 10.1021/ja403002m. [DOI] [PubMed] [Google Scholar]
  13. Wang H.; Li B.; Wu H.; Hu T. L.; Yao Z.; Zhou W.; Xiang S.; Chen B. L. A Flexible Microporous Hydrogen-Bonded Organic Framework for Gas Sorption and Separation. J. Am. Chem. Soc. 2015, 137, 9963–9970. 10.1021/jacs.5b05644. [DOI] [PubMed] [Google Scholar]
  14. Anderson S. L.; Boyd P. G.; Gładysiak A.; Nguyen T. N.; Palgrave R. G.; Kubicki D.; Emsley L.; Bradshaw D.; Smit M. J.; Stylianou K. C.; Rosseinsky B. Nucleobase Pairing and Photodimerization in a Biologically Derived Metal-Organic Framework Nanoreactor. Nat. Commun. 2019, 10, 1612 10.1038/s41467-019-09486-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Stylianou K. C.; Warren J. E.; Chong S. Y.; Rabone J.; Bacsa J.; Bradshaw D.; Rosseinsky M. J. CO2 Selectivity of a 1D Microporous Adenine-Based Metal–Organic Framework Synthesized in Water. Chem. Commun. 2011, 47, 3389–3391. 10.1039/c0cc05559j. [DOI] [PubMed] [Google Scholar]
  16. Rabone J.; Yue Y.-F.; Chong S.; Stylianou K. C.; Bacsa J.; Bradshaw D.; Darling G. R.; Berry N. G.; Khimyak Y. Z.; Ganin A. Y.; Wiper P.; Claridge J. B.; Rosseinsky M. J. An Adaptable Peptide-Based Porous Material. Science 2010, 329, 1053–1057. 10.1126/science.1190672. [DOI] [PubMed] [Google Scholar]
  17. Katsoulidis A. P.; Antypov D.; Whitehead G. F. S.; Carrington E. J.; Adams D. J.; Berry N. G.; Darling G. R.; Dyer M. S.; Rosseinsky M. J. Chemical Control of Structure and Guest Uptake by a Conformationally Mobile Porous Material. Nature 2019, 565, 213–217. 10.1038/s41586-018-0820-9. [DOI] [PubMed] [Google Scholar]
  18. Katsoulidis A. P.; Park K. S.; Antypov D.; Martí-Gastaldo C.; Miller G. J.; Warren J. E.; Robertson C. M.; Blanc F.; Darling G. R.; Berry N. G.; Purton J. A.; Adams D. J.; Rosseinsky M. J. Guest-Adaptable and Water-Stable Peptide-Based Porous Materials by Imidazolate Side Chain Control. Angew. Chem., Int. Ed. 2014, 53, 193–198. 10.1002/anie.201307074. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Bracco S.; Asnaghi D.; Negroni M.; Sozzani P.; Comotti A. Porous Dipeptide Crystals as Volatile-Drug Vessels. Chem. Commun. 2018, 54, 148–151. 10.1039/C7CC06534E. [DOI] [PubMed] [Google Scholar]
  20. Görbitz C. H. Microporous Organic Materials from Hydrophobic Dipeptides. Chem. - Eur. J. 2007, 13, 1022–1031. 10.1002/chem.200601427. [DOI] [PubMed] [Google Scholar]
  21. Görbitz C. H. Nanotube Formation by Hydrophobic Dipeptides. Chem. - Eur. J. 2001, 7, 5153–5159. . [DOI] [PubMed] [Google Scholar]
  22. Görbitz C. H. The Structure of Nanotubes Formed by Diphenylalanine, the Core Recognition Motif of Alzheimer’s β-Amyloid Polypeptide. Chem. Commun. 2006, 2332–2334. 10.1039/B603080G. [DOI] [PubMed] [Google Scholar]
  23. Tao K.; Makam P.; Aizen R.; Gazit E. Self-Assembling Peptide Semiconductors. Science 2017, 358, eaam9756 10.1126/science.aam9756. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Tao K.; Wang J.; Zhou P.; Wang C.; Xu H.; Zhao X.; Lu J. R. Self-Assembly of Short Aβ(16-22) Peptides: Effect of Terminal Capping and the Role of Electrostatic Interaction. Langmuir 2011, 27, 2723–2730. 10.1021/la1034273. [DOI] [PubMed] [Google Scholar]
  25. Spackman M. A.; Jayatilaka D. Hirshfeld Surface Analysis. CrystEngComm 2009, 11, 19–32. 10.1039/B818330A. [DOI] [Google Scholar]
  26. Berger O.; Gazit E. Molecular Self-Assembly Using Peptide Nucleic Acids. Pept. Sci. 2017, 108, e22930 10.1002/bip.22930. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Egholm M.; Buchardt O.; Nielsen P. E.; Berg R. H. Peptide Nucleic Acids (PNA). Oligonucleotide Analogs with an Achiral Peptide Backbone. J. Am. Chem. Soc. 1992, 114, 1895–1897. 10.1021/ja00031a062. [DOI] [Google Scholar]
  28. Buchardt O.; Egholm M.; Nielsen P. E.; Berg R. H.. Peptide Nucleic Acids Having Amino Acid Side Chains. U.S. Patent US5,719,262A,1998.
  29. Berger O.; Adler-Abramovich L.; Levy-Sakin M.; Grunwald A.; Liebes-Peer Y.; Bachar M.; Buzhansky L.; Mossou E.; Forsyth V. T.; Schwartz T.; Ebenstein Y.; Frolow F.; Shimon L. J. W.; Patolsky F.; Gazit E. Light-Emitting Self-Assembled Peptide Nucleic Acids Exhibit Both Stacking Interactions and Watson-Crick Base Pairing. Nat. Nanotechnol. 2015, 10, 353–360. 10.1038/nnano.2015.27. [DOI] [PubMed] [Google Scholar]
  30. Gao J.; Zhang W.; Wu Z.; Zheng Y.; Fu D. Enantiomorphic Perovskite Ferroelectrics with Circularly Polarized Luminescence. J. Am. Chem. Soc. 2020, 142, 4756–4761. 10.1021/jacs.9b13291. [DOI] [PubMed] [Google Scholar]
  31. Gan Z.; Wu X.; Zhu X.; Shen J. Light-Induced Ferroelectricity in Bioinspired Self-Assembled Diphenylalanine Nanotubes/Microtubes. Angew. Chem., Int. Ed. 2013, 52, 2055–2059. 10.1002/anie.201207992. [DOI] [PubMed] [Google Scholar]
  32. Tao K.; Xue B.; Li Q.; Hu W.; Shimon L. J. W.; Makam P.; Si M.; Yan X.; Zhang M.; Cao Y.; Yang R. S.; Li J. B.; Gazit E. Stable and Optoelectronic Dipeptide Assemblies for Power Harvesting. Mater. Today 2019, 30, 10–16. 10.1016/j.mattod.2019.04.002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Knowles T. P.; Fitzpatrick A. W.; Meehan S.; Mott H. R.; Vendruscolo M.; Dobson C. M.; Welland M. E. Role of Intermolecular Forces in Defining Material Properties of Protein Nanofibrils. Science 2007, 318, 1900–1903. 10.1126/science.1150057. [DOI] [PubMed] [Google Scholar]
  34. Herling T. W.; Garcia G. A.; Michaels T. C.; Grentz W.; Dean J.; Shimanovich U.; Gang H.; Müller T.; Kav B.; Terentjev E. M.; Dobson C. M.; Knowles T. P. J. Force Generation by the Growth of Amyloid Aggregates. Proc. Natl. Acad. Sci. U.S.A. 2015, 112, 9524–9529. 10.1073/pnas.1417326112. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Tao K.; Hu W.; Xue B.; Chovan D.; Brown N.; Shimon L. J. W.; Maraba O.; Cao Y.; Tofail S. A.; Thompson D.; Li J. B.; Yang R. S.; Gazit E. Bioinspired Stable and Photoluminescent Assemblies for Power Generation. Adv. Mater. 2019, 31, 1807481 10.1002/adma.201807481. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Knowles T. P.; Buehler M. J. Nanomechanics of Functional and Pathological Amyloid Materials. Nat. Nanotechnol. 2011, 6, 469–479. 10.1038/nnano.2011.102. [DOI] [PubMed] [Google Scholar]
  37. Zelenovskiy P.; Kornev I.; Vasilev S.; Kholkin A. On the Origin of the Great Rigidity of Self-Assembled Diphenylalanine Nanotubes. Phys. Chem. Chem. Phys. 2016, 18, 29681–29685. 10.1039/C6CP04337B. [DOI] [PubMed] [Google Scholar]
  38. Zhao Y.; Ge Z.; Fang J. Elastic Modulus of Viral Nanotubes. Phys. Rev. E 2008, 78, 031914 10.1103/PhysRevE.78.031914. [DOI] [PubMed] [Google Scholar]
  39. Xu Z.; Paparcone R.; Buehler M. J. Alzheimer’s Aβ(1-40) Amyloid Fibrils Feature Size-Dependent Mechanical Properties. Biophys. J. 2010, 98, 2053–2062. 10.1016/j.bpj.2009.12.4317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Yogurtcu O. N.; Wolgemuth C. W.; Sun S. X. Mechanical Response and Conformational Amplification in α-Helical Coiled Coils. Biophys. J. 2010, 99, 3895–3904. 10.1016/j.bpj.2010.10.002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. López-García P.; Goktas M.; Bergues-Pupo A. E.; Koksch B.; Silva D. V.; Blank K. G. Structural Determinants of Coiled Coil Mechanics. Phys. Chem. Chem. Phys. 2019, 21, 9145–9149. 10.1039/C9CP00665F. [DOI] [PubMed] [Google Scholar]
  42. Bera S.; Mondal S.; Xue B.; Shimon L. J. W.; Cao Y.; Gazit E. Rigid helical-like assemblies from a self-aggregating tripeptide. Nat. Mater. 2019, 18, 503–509. 10.1038/s41563-019-0343-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Baimpos T.; Nikolakis V.; Kouzoudis D. Measurement of the Elastic Properties of Zeolite Films Using Metglas-Zeolite Composite Sensors. Stud. Surf. Sci. Catal. 2008, 174, 665–668. 10.1016/S0167-2991(08)80286-8. [DOI] [Google Scholar]
  44. Tan J. C.; Cheetham A. K. Mechanical Properties of Hybrid Inorganic-Organic Framework Materials: Establishing Fundamental Structure-Property Relationships. Chem. Soc. Rev. 2011, 40, 1059–1080. 10.1039/c0cs00163e. [DOI] [PubMed] [Google Scholar]
  45. Rogge S. M. J.; Waroquier M.; Speybroeck V. V. Reliably Modeling the Mechanical Stability of Rigid and Flexible Metal-Organic Frameworks. Acc. Chem. Res. 2018, 51, 138–148. 10.1021/acs.accounts.7b00404. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Ortiz A. U.; Boutin A.; Fuchs A. H.; Coudert F.-X. Anisotropic Elastic Properties of Flexible Metal-Organic Frameworks: How Soft are Soft Porous Crystals?. Phys. Rev. Lett. 2012, 109, 195502 10.1103/PhysRevLett.109.195502. [DOI] [PubMed] [Google Scholar]
  47. Nikitin T.; Kopyl S.; Shur V. Y.; Kopelevich Y. V.; Kholkin A. L. Low-Temperature Photoluminescence in Self-Assembled Diphenylalanine Microtubes. Phys. Lett. A 2016, 380, 1658–1662. 10.1016/j.physleta.2016.02.043. [DOI] [Google Scholar]
  48. Amdursky N.; Beker P.; Koren I.; Bank-Srour B.; Mishina E.; Semin S.; Rasing T.; Rosenberg Y.; Barkay Z.; Gazit E.; Rosenman G. Structural Transition in Peptide Nanotubes. Biomacromolecules 2011, 12, 1349–1354. 10.1021/bm200117w. [DOI] [PubMed] [Google Scholar]
  49. Tao K.; Donnell J. O’.; Yuan H.; Haq E. U.; Guerin S.; Shimon L. J. W.; Xue B.; Silien C.; Cao Y.; Thompson D.; Yang R.; Tofail S. A. M.; Gazit E. Accelerated Charge Transfer in Water-Layered Peptide Assemblies. Energy Environ. Sci. 2020, 13, 96–101. 10.1039/C9EE02875G. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Tao K.; Xue B.; Frere S.; Slutsky I.; Cao Y.; Wang W.; Gazit E. Multiporous Supramolecular Microspheres for Artificial Photosynthesis. Chem. Mater. 2017, 29, 4454–4460. 10.1021/acs.chemmater.7b00966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Tao K.; Fan Z.; Sun L.; Makam P.; Tian Z.; Ruegsegger M.; Shaham-Niv S.; Hansford D.; Aizen R.; Pan Z.; Galster S.; Ma J.; Yuan F.; Su M.; Qu S.; Zhang M.; Gazit E.; Li J. B. Quantum Confined Peptide Assemblies with Tunable Visible to Near-Infrared Spectral Range. Nat. Commun. 2018, 9, 3217 10.1038/s41467-018-05568-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Kim S.; Kim J. H.; Lee J. S.; Park C. B. Beta-Sheet-Forming, Self-Assembled Peptide Nanomaterials towards Optical, Energy, and Healthcare Applications. Small 2015, 11, 3623–3640. 10.1002/smll.201500169. [DOI] [PubMed] [Google Scholar]
  53. Sun B.; Tao K.; Jia Y.; Yan X.; Zou Q.; Gazit E.; Li J. B. Photoactive Properties of Supramolecular Assembled Short Peptides. Chem. Soc. Rev. 2019, 48, 4387–4400. 10.1039/C9CS00085B. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Lee S. H.; Kim J. H.; Park C. B. Coupling Photocatalysis and Redox Biocatalysis toward Biocatalyzed Artificial Photosynthesis. Chem. - Eur. J. 2013, 19, 4392–4406. 10.1002/chem.201204385. [DOI] [PubMed] [Google Scholar]
  55. Kresse G.; Furthmüller J. Efficiency of Ab-Initio Total Energy Calculations for Metals and Semiconductors Using a Plane-Wave Basis Set. Comput. Mater. Sci. 1996, 6, 15–50. 10.1016/0927-0256(96)00008-0. [DOI] [PubMed] [Google Scholar]
  56. Kresse G.; Joubert D. From Ultrasoft Pseudopotentials to the Projector Augmented-Wave Method. Phys. Rev. B 1999, 59, 1758. 10.1103/PhysRevB.59.1758. [DOI] [Google Scholar]
  57. Hohenberg P.; Kohn W. Inhomogeneous Electron Gas. Phys. Rev. 1964, 136, B864. 10.1103/PhysRev.136.B864. [DOI] [Google Scholar]
  58. Kohn W.; Sham L. J. Self-Consistent Equations Including Exchange and Correlation Effects. Phys. Rev. 1965, 140, A1133. 10.1103/PhysRev.140.A1133. [DOI] [Google Scholar]
  59. Perdew J. P.; Burke K.; Ernzerhof M. Generalized Gradient Approximation Made Simple. Phys. Rev. Lett. 1996, 77, 3865. 10.1103/PhysRevLett.77.3865. [DOI] [PubMed] [Google Scholar]
  60. Heyd J.; Scuseria G. E.; Ernzerhof M. Hybrid Functionals Based on a Screened Coulomb Potential. J. Chem. Phys. 2003, 118, 8207 10.1063/1.1564060. [DOI] [Google Scholar]
  61. Krukau A. V.; Vydrov O. A.; Izmaylov A. F.; Scuseria G. E. Influence of the Exchange Screening Parameter on the Performance of Screened Hybrid Functionals. J. Chem. Phys. 2006, 125, 224106 10.1063/1.2404663. [DOI] [PubMed] [Google Scholar]
  62. Klimeš J.; Bowler D. R.; Michaelides A. Van der Waals Density Functionals Applied to Solids. Phys. Rev. B 2011, 83, 195131 10.1103/PhysRevB.83.195131. [DOI] [Google Scholar]
  63. Turner M. J.; McKinnon J. J.; Wolff S. K.; Grimwood D. J.; Spackman P. R.; Jayatilaka D.; Spackman M. A.. CrystalExplorer17; University of Western Australia. http://hirshfeldsurface.net., 2017.

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

am0c13295_si_001.pdf (2.7MB, pdf)

Articles from ACS Applied Materials & Interfaces are provided here courtesy of American Chemical Society

RESOURCES