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Rotary FoF1-ATP Synthase-Driven Flasklike Pentosan Colloidal Motors with ATP Synthesis and Storage

Cite this: J. Am. Chem. Soc. 2024, 146, 16, 11245–11253
Publication Date (Web):April 10, 2024
https://doi.org/10.1021/jacs.4c00334
Copyright © 2024 American Chemical Society

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    Abstract

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    We report the hierarchical assembly of a chloroplast-derived rotary FoF1-ATPase motor-propelled flasklike pentosan colloidal motor (FPCM) with the ability of the synthesis, storage, and triggered release of biological energy currency ATP. These streamlined and submicrometer-sized hollow flasklike pentosan colloidal motors are prepared by combining a soft-template-based hydrothermal polymerization with a vacuum infusion of chloroplast-derived proteoliposomes containing rotary FoF1-ATPase motors. The generation of proton motive force across the proteoliposomes by injecting an acidic buffer solution promotes the rotation of FoF1-ATPase motors to drive the self-propelled motion of FPCMs, accompanying the inner ATP synthesis and storage. These rotary FoF1-ATPase motor-powered FPCMs exhibit a chemotactic behavior by migrating from their neck opening to their round bottom along a proton gradient of the external environment (negative chemotaxis). Such rotary biomolecular motor-driven flasklike pentosan colloidal motors with ATP synthesis and on-demand release make them promising candidates for engineering novel intelligent nanocarriers to actively regulate cellular metabolism.

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    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/jacs.4c00334.

    • Descriptions of additional data; TEM image and DLS analysis of thylakoid vesicles; optical microscopy images, of chloroplasts, thylakoids, and RBMPs; TEM and AFM image of the RBMPs; ATP production in the inner or outer of RBMPs; schematic illustration of the fabrication process of the FPCPs and chemical structures; SEM image of the FPCPs; TEM images of RBMPs before and after the ultrasonic process; ATP production in the inner of RBMPs before and after the ultrasonic process; ζ-potential measurements of FPCPs, RBMPs, and FPCMs; time-lapse images of the motion behavior of FPCMs for 30 s; enlarged screenshot of the trajectories of FPCMs showing the direction of motion in 6 s; motion trajectory of FPCMs under different reaction conditions in 8 s; fluorescence spectra and sigmoidal behavior of pyranine (8-hydroxy-1,3,6-pyrenetrisulfonate); fluorescence spectra of pyranine (8-hydroxy-1,3,6-pyrenetrisulfonate) at the external and internal of FPCMs; ζ-potential measurements of FPCPs, RBMPs, and FPCMs in acidic buffer solution; trajectories of the FPCPs + pH gradient, FPCPs + liposomes + pH gradient, and FPCPs + RBMPs + pH gradient in 10 s; drift velocity of FPCMs at different distances from the acidic buffer source; negative CI index of FPCMs during the chemotactic process (PDF)

    • Motion behavior of FPCMs during ATP synthesis inside for 4 s (Video S1) (MP4)

    • Brownian motion of FPCMs for 4 s (Video S2) (MP4)

    • Trajectories for the negative chemotaxis of the FPCMs with a color-coded average speed in 5 s and with a color-coded time in 1 s under proton gradient generated from the top side (Video S3) (MP4)

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