Piezoelectricity of the Transmembrane Protein ba3 Cytochrome c Oxidase

Joseph O'Donnell, Pierre André Cazade, Sarah Guerin, Ahmed Djeghader, Ehtsham Ul Haq, Kai Tao, Ehud Gazit, Eiichi Fukada, Christophe Silien, Tewfik Soulimane*, Damien Thompson*, Syed A.M. Tofail*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

Abstract

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.

Original languageEnglish
Article number2100884
JournalAdvanced Functional Materials
Volume31
Issue number28
DOIs
StatePublished - 9 Jul 2021

Funding

FundersFunder number
Higher
Higher Education Authority Irish Center for High‐End Computing
Science Foundation Ireland12/RC/2275_P2, 15/CDA/3491
Irish Research CouncilGOIPG/2018/1161
Irish Centre for High-End Computing12/RI/2345/SOF

    Keywords

    • functional biomaterials
    • materials design
    • organic piezoelectrics
    • piezoresponse force microscopy
    • predictive modeling
    • transmembrane proteins

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