Accelerated charge transfer in water-layered peptide assemblies

Tao, Kai; O'Donnell, Joseph; Yuan, Hui; Haq, Ehtsham Ul; Guerin, Sarah; Shimon, Linda J. W.; Xue, Bin; Silien, Christophe; Cao, Yi; Thompson, Damien; Yang, Rusen; Tofail, Syed A. M.; Gazit, Ehud

doi:10.1039/c9ee02875g

Cited by 42 publications

(27 citation statements)

References 37 publications

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“…As proteins hardly contribute to the crystal dipole moment in ba 3 cytochrome c oxidase (Table S1, Supporting Information), the structuration of water around the protein units is the most likely driving force behind the crystal dipole moments and its variation under strain, which results in the electromechanical response. Similar to recent discoveries of enhanced piezoelectricity in peptide crystals with ordered water layers, [ 33 ] resculpting the solute‐templated water structure may be key to producing strong piezoelectricity in bio‐assemblies ( Figure ).…”

Section: Modeling‐assisted Placement Of Membrane Proteins In the Biopiezoelectric Hierarchymentioning

confidence: 55%

Piezoelectricity of the Transmembrane Protein ba₃ Cytochrome c Oxidase

O'Donnell

Cazade

Guerin

et al. 2021

Adv Funct Materials

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Controlling the electromechanical response of piezoelectric biological structures including tissues, peptides, and amino acids provides new applications for biocompatible, sustainable materials in electronics and medicine. Here, the piezoelectric effect is revealed in another class of biological materials, with robust longitudinal and shear piezoelectricity measured in single crystals of the transmembrane protein ba3 cytochrome c oxidase from Thermus thermophilus. The experimental findings from piezoresponse force microscopy are substantiated using a range of control measurements and molecular models. The observed longitudinal and shear piezoelectric responses of ≈2 and 8 pm V−1, respectively, are comparable to or exceed the performance of commonly used inorganic piezoelectric materials including quartz, aluminum nitride, and zinc oxide. This suggests that transmembrane proteins may provide, in addition to physiological energy transduction, technologically useful piezoelectric material derived entirely from nature. Membrane proteins could extend the range of rationally designed biopiezoelectric materials far beyond the minimalistic peptide motifs currently used in miniaturized energy harvesters, and the finding of robust piezoelectric response in a transmembrane protein also raises fundamental questions regarding the molecular evolution, activation, and role of regulatory proteins in the cellular nanomachinery, indicating that piezoelectricity might be important for fundamental physiological processes.

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Section: Modeling‐assisted Placement Of Membrane Proteins In the Biopiezoelectric Hierarchymentioning

confidence: 55%

Piezoelectricity of the Transmembrane Protein ba₃ Cytochrome c Oxidase

O'Donnell

Cazade

Guerin

et al. 2021

Adv Funct Materials

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Section: Results and Discussionmentioning

confidence: 99%

“…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 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.…”

Section: ■ Introductionmentioning

confidence: 99%

Bioinspired Suprahelical Frameworks as Scaffolds for Artificial Photosynthesis

Tao

Xue

Han³

et al. 2020

ACS Appl. Mater. Interfaces

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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.

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“…When the temperature further increased up to 580 K, an abrupt drop was observed in the fractions of c ‐WW H‐bonds and π–π stacking, from 75 % and 90 %, respectively, to nearly 0 % (Figure a), demonstrating the transition of the crystal structures to amorphous states (Figure d). Notably, the calculated transition temperature was lower than that measured using TGA, probably since the parameters of water molecules used in the simulations were derived from the bulky water system, while the crystallized water molecules are actually in interfacial states, which can form stronger H‐bonds compared to the bulky ones . This structural transition was accompanied by an increase of the simulation box volume, from 544 nm 3 at 300 K to 570 nm 3 at 500 K and 690 nm 3 at 580 K (Figure e).…”

Section: Figurementioning

confidence: 87%

Bioinspired Supramolecular Packing Enables High Thermo‐Sustainability

et al. 2020

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Bottom-up self-assembled bioinspired materials have attracted increasing interest in a variety fields. The use of peptide supramolecular semiconductors for optoelectronic applications is especially intriguing. However, the characteristic thermal unsustainability limits their practical application. Here, we report the thermal sustainability of cyclo-ditryptophan assemblies up to 680 K. Non-covalent interactions underlie the stability mechanism, generating a low excitonbinding energy of only 0.29 eV and a high thermal-quenchingactivation energy of up to 0.11 eV. The contributing forces comprise predominantly of aromatic interactions, followed by hydrogen bonding between peptide molecules, and, to a lesser extent, water-mediated associations. This thermal sustainability results in a temperature-dependent conductivity of the supramolecular semiconductors, showing 93 % reduction of the resistance from 320 K to 440 K. Our results establish thermosustainable peptide self-assembly for heat-sensitive applications.

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Accelerated charge transfer in water-layered peptide assemblies

Abstract: An aromatic dipeptide crystallizes into sandwich-like supramolecular semiconductors comprising alternating water and peptide layers, allowing doping and facilitating charge transfer.

Cited by 42 publications

References 37 publications

Piezoelectricity of the Transmembrane Protein ba₃ Cytochrome c Oxidase

Piezoelectricity of the Transmembrane Protein ba₃ Cytochrome c Oxidase

Bioinspired Suprahelical Frameworks as Scaffolds for Artificial Photosynthesis

Bioinspired Supramolecular Packing Enables High Thermo‐Sustainability

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Accelerated charge transfer in water-layered peptide assemblies

Abstract: An aromatic dipeptide crystallizes into sandwich-like supramolecular semiconductors comprising alternating water and peptide layers, allowing doping and facilitating charge transfer.

Cited by 42 publications

References 37 publications

Piezoelectricity of the Transmembrane Protein ba3 Cytochrome c Oxidase

Piezoelectricity of the Transmembrane Protein ba3 Cytochrome c Oxidase

Bioinspired Suprahelical Frameworks as Scaffolds for Artificial Photosynthesis

Bioinspired Supramolecular Packing Enables High Thermo‐Sustainability

Contact Info

Product

Resources

About

Piezoelectricity of the Transmembrane Protein ba₃ Cytochrome c Oxidase

Piezoelectricity of the Transmembrane Protein ba₃ Cytochrome c Oxidase