Accelerated charge transfer in water-layered peptide assemblies

Abstract

Bioinspired assemblies bear massive potential for energy generation and storage. Yet, biological molecules have severe limitations for charge transfer. Here, we report l-tryptophan-d-tryptophan assembling architectures comprising alternating water and peptide layers. The extensive connection of water molecules results in significant dipole-dipole interactions and piezoelectric response that can be further engineered by doping via iodine adsorption or isotope replacement with no change in the chemical composition. This simple system and the new doping strategies supply alternative solutions for enhancing charge transfer in bioinspired supramolecular architectures.

Fig. 1. Crystallographic structure of water-enriched Ww assemblies.

(a) scanning electron microscopy image of Ww crystals. (b) Optical microscopy image of a Ww crystal labelled with the crystallographic dimensions. Magnification scale: X60. (c) Monomeric structure of the crystal, showing one dipeptide building block incorporating four water molecules by hydrogen bonding. The water molecules are numbered for clarity. Adopted from ref. . (d) Hydrophilic/hydrophobic partitioning and layering in the Ww crystal. The hydrophilic section composed of a water layer and the peptide backbone is shaded in blue and the hydrophobic section comprising side-chain indole rings is shaded in red. Zoom-in panel “1”: a lateral view of the peptide assembly with water molecules strung along the b axis. The hydrogen bonds are labelled in different colours to highlight their distinct roles in the system. The green set composes a large channel, the magenta group comprises a small channel, and the blue subgroup provides support by bridging the adjacent monomers. Panel “2”: top view of the two channels composed of hydrogen bonds between peptide backbones and water molecules. The large and small channels are shaded in green and magenta, respectively, consistent with the corresponding hydrogen bonds. Panel “3”–“4”: front and side view, respectively, of the water layer in the crystal. Panel “5”: magnified view of the hydrophobic region composed of side-chain indole rings. The two types of aromatic interactions are indicated in red and green, respectively, with the dihedral angle and nearest atomic distance labelled. The carbon, nitrogen and oxygen atoms are represented as grey, blue and red spheres, respectively. The hydrogen atoms are omitted for clarity, and the hydrogen bonds are labelled between the donor and acceptor atoms.

Fig. 2. Doping of Ww crystals through iodine adsorption and introduction of neutrons.

(a) The electronic band structure of Ww crystals calculated by density functional theory. (b) UV-vis absorbance spectra of Ww crystals before (blue) and after (red) doping with iodine. The reference absorption of iodine alone (black) is shown for comparison. (c) Mass spectrometry of Ww crystals before (upper panel) and after (lower panel) doping with iodine, showing the same molecular weights. The insets show photographs of the peptide crystals before and after iodine doping. (d) Crystallographic structure of Ww crystals prepared in deuterium oxide. (e) Crystallographic data collection table of Ww crystals in normal water and in deuterium oxide, showing nearly-identical crystal parameters.

Fig. 3. Doping-enhanced charge transfer of Ww crystals.

(a) Crystallographic structure showing the side-chain indole rings of Ww surrounded by a hydrogen-bonded, motion-restricted medium composed of water molecules and polar atoms (oxygen, nitrogen) of peptide backbones. (b) Fluorescent microscopy images of pristine Ww crystals (upper row; scale bar = 30 μm), doped with iodine (middle row; scale bar: 50 μm) and with neutrons (lower row; scale bar = 200 μm), showing the attenuated fluorescence upon doping. DIC: differential interference contrast mode; dapi: 4′,6-diamidino-2-phenylindole filter (Ex: 340–380 nm, Em: 435–485 nm); CFP: cyan fluorescent protein filter (Ex: 420–445 nm, Em: 460–510 nm); GFP: green fluorescent protein filter (Ex: 455–485 nm, Em: 500–545 nm); CY3: cyanine 3 filter (Ex: 528–553 nm, Em: 590–650 nm). (c) Maximal emission of pristine Ww crystals vs. the excitation wavelength, showing a characteristic linear relationship. (d) Schematic representation showing the continuous medium relaxation surrounding the indole rings in pristine (upper panel) and doped (lower panel) Ww crystals. The “I state” refers to one of the intermediate states between the initial excited state (FC state) and the final solvent relaxed state (R state). v₀, v_i and v_R represent the frequencies corresponding to the FC, I and R states, respectively, while λ_C and λ_R denote the maximal emission wavelengths associated with these states. (e) Maximal emission spectra of pristine (black), iodine-(red) and neutron-(blue) doped Ww crystals upon excitation at 330 nm. (f) Table summarizing the proton conductivity of pristine and doped Ww crystals at different temperatures and 98% RH. (g) Schematic illustration of proton translocation along the hydrogen-bonded water molecule chain inside the Ww crystals, following the Grotthuss mechanism. The moving hydrogen nucleus is labelled in blue.

Fig. 4. Doping-mediated piezoelectricity enhancement of Ww crystals.

(a) Comparison of the d₃₃ coefficients of pristine and doped Ww crystals measured using PFM. (b) Comparison of d₃₃ coefficients among different classes of organic and inorganic materials. The magenta, blue, cyan and grey regions show the range of d₃₃ values for peptide/amino acid self-assemblies, non-peptide organic materials, organic–inorganic hybrids and inorganic constituents, respectively. The Ww series (pristine and doped with iodine or neutrons) are denoted in red for comparison. From left to right: M13 bacteriophage nanopillars (phage-p), γ-glycine (γ-G), dl-alanine (dl-A), FF microrod arrays prepared using electric field (FF array-E), FF microrod arrays (FF array), M13 bacteriophage thin films (phage-f) and type I collagen films (collagen); nylon, Rochelle salt (E337) and triglycine sulfate (TGS), diisopropylammonium bromide (DIPAB), croconic acid (CRCA), poly(vinylidene fluoride) (PVDF), poly(vinylidene fluoride/trifluoroerhylene) (P(VDF-TrFE)), imidazolium perchlorate (Im-ClO₃); trimethylchloromethyl ammonium trichloromanganese(ii) (TMCM-MnCl₃); ZnO and CdS, periodically poled lithium niobate (LiNbO₃), potassium titanyl phosphate (KTP), non-poled and poled BaTiO₃ [001], lead zirconate titanate (PZT). (c) Schematic cross-section diagram of the proof-of-concept generator used as a direct power source comprising the peptide crystals as the active components. The inset shows a photographic picture of the device. (d) Comparison of the output signals (V_oc, I_sc) from the generators utilized as a direct power source using undoped or doped Ww crystals as the active components, as designed in (c).