Light-controlled micron-scale molecular motion

ABSTRACT The micron-scale movement of biomolecules along supramolecular pathways, mastered by nature, is a remarkable system requiring strong yet reversible interactions between components

under the action of a suitable stimulus. Responsive microscopic systems using a variety of stimuli have demonstrated impressive relative molecular motion. However, locating the position of a

movable object that travels along self-assembled fibres under an irresistible force has yet to be achieved. Here, we describe a purely supramolecular system where a molecular ‘traveller’

moves along a ‘path’ over several microns when irradiated with visible light. Real-time imaging of the motion in the solvated state using total internal reflection fluorescence microscopy

shows that anionic porphyrin molecules move along the fibres of a bis-imidazolium gel upon irradiation. Slight solvent changes mean movement and restructuring of the fibres giving

microtoroids, indicating control of motion by fibre mechanics with solvent composition. The insight provided here may lead to the development of artificial travellers that can perform

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SIMILAR CONTENT BEING VIEWED BY OTHERS SELF-REGULATED NON-RECIPROCAL MOTIONS IN SINGLE-MATERIAL MICROSTRUCTURES Article 04 May 2022 EXERTING PULLING FORCES IN FLUIDS BY DIRECTIONAL

DISASSEMBLY OF MICROCRYSTALLINE FIBRES Article Open access 29 July 2024 PROPAGATING WAVE IN A FLUID BY COHERENT MOTION OF 2D COLLOIDS Article Open access 19 November 2021 DATA AVAILABILITY

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_J. Phys. D-Appl. Phys._ 52, 163001 (2019). Article  CAS  Google Scholar  Download references ACKNOWLEDGEMENTS All the authors thank the School of Life Sciences Imaging (SLIM) in Nottingham

for access to the optical microscope and the Nanoscale and Microscale Research Centre (nmRC) for facilitating access to electron microscopes. D.B.A. thanks the Telluride Conference on

Molecular Rotors, Motors, and Switches for inspiring this research. We warmly thank M. Amabilino i Pérez for assistance with graphics (D.B.A.). A.R.M. acknowledges funding from the European

Union’s Horizon 2020 research and innovation programme under Marie–Skłodowska–Curie grant agreement no. 793424. The microscope facility was established using the BB/L013827/1 fund. This work

was supported by the Engineering and Physical Sciences Research Council (EPSRC) under grants EP/M005178/1 and EP/N024818/1 (D.B.A.), EU ERDF (FEDER) funds, Spanish Government grants

TEC2017-85059-C3-2-R and PID2020-115663GB-C3-2 (L.P.-G.) and the University of Nottingham (B.B., M.S.) including work under the Anne McLaren fellowship scheme (L.P.-G.) and the Propulsion

Futures Beacon of Excellence (D.B.A.). AUTHOR INFORMATION Author notes * Mario Samperi Present address: Istituto di Tecnologie Avanzate per l’Energia “Nicola Giordano” - CNR-ITAE, Messina,

Italy AUTHORS AND AFFILIATIONS * School of Pharmacy, University of Nottingham, Nottingham, United Kingdom Mario Samperi & Lluïsa Pérez-García * School of Chemistry, GSK Carbon Neutral

Laboratories for Sustainable Chemistry, University of Nottingham, Nottingham, United Kingdom Mario Samperi, Bilel Bdiri, Charlotte D. Sleet, Ajith R. Mallia & David B. Amabilino * SLIM

Imaging Unit, School of Life Sciences, University of Nottingham, Nottingham, United Kingdom Robert Markus * Departament de Farmacologia, Toxicologia i Química Terapèutica, Universitat de

Barcelona, Barcelona, Spain Lluïsa Pérez-García * Institut de Nanociència i Nanotecnologia IN2UB, Universitat de Barcelona, Barcelona, Spain Lluïsa Pérez-García Authors * Mario Samperi View

author publications You can also search for this author inPubMed Google Scholar * Bilel Bdiri View author publications You can also search for this author inPubMed Google Scholar * Charlotte

D. Sleet View author publications You can also search for this author inPubMed Google Scholar * Robert Markus View author publications You can also search for this author inPubMed Google

Scholar * Ajith R. Mallia View author publications You can also search for this author inPubMed Google Scholar * Lluïsa Pérez-García View author publications You can also search for this

author inPubMed Google Scholar * David B. Amabilino View author publications You can also search for this author inPubMed Google Scholar CONTRIBUTIONS Author contributions are defined based

on the CRediT (Contributor Roles Taxonomy) and listed alphabetically. Conceptualization: D.B.A. and L.P.-G. Data curation: M.S. Formal analysis: M.S., D.B.A. and L.P.-G. Funding acquisition:

D.B.A. and L.P.-G. Investigation: M.S., B.B., A.R.M., R.M. and C.D.S. Methodology: D.B.A., M.S., R.M. and L.P.-G. Project administration: D.B.A. and L.P.-G. Supervision: D.B.A. and L.P.-G.

Validation: D.B.A. and L.P.-G. Writing original draft: M.S., D.B.A. and L.P.-G. Writing review and editing: M.S., L.P.-G. and D.B.A. CORRESPONDING AUTHOR Correspondence to David B.

Amabilino. ETHICS DECLARATIONS COMPETING INTERESTS The authors declare no competing interests. ADDITIONAL INFORMATION PEER REVIEW INFORMATION _Nature Chemistry_ thanks the anonymous

reviewers for their contribution to the peer review of this work. PUBLISHER’S NOTE Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional

affiliations. EXTENDED DATA EXTENDED DATA FIG. 1 GEL FORMATION. (A) A picture of gel samples of 1·2Br obtained with water:ethanol ratio 5:5 without guest molecules (Gel), with incorporated

azobenzene (Gel@Azo), porphyrin (Gel@TCPP) and both (Gel@TCPP@Azo). The scale bar represents 1 cm. Gel samples were always prepared by addition of MilliQ water to an ethanolic solution of

1·2Br, giving a final amphiphile concentration of 8 mM. For TCPP-containing gels, aqueous solutions of the TCPP sodium salt were prepared by dispersing the desired amount of solid TCPP in

water followed by the addition of 4 equivalents of sodium hydroxide (from a 0.1 M stock solution). For AZO-containing gels, an ethanolic solution of 4-(phenylazo)benzoic acid (AZO)was

premixed with 1·2Br, and the equimolar equivalent of sodium hydroxide was added in water in order to incorporate the AZO as its sodium salt. The final concentration of TCPP and AZO within

the gels was always 60 μM and 2 mM, respectively. (B) Gelation time of the samples at room temperature (approximately 22 °C) obtained with solvent ratio 5:5 (blue bars) and 7:3 (red bars).

EXTENDED DATA FIG. 2 RHEOLOGY OF THE MULTICOMPONENT GELS. Shear stress profiles displaying storage (G’, black curve) and loss (G”, red curve) moduli obtained for gels in water-ethanol ratio

5:5 (top box) and 7:3 (bottom box). EXTENDED DATA FIG. 3 X-RAY POWDER DIFFRACTOGRAMS OF XEROGELS. X-ray powder diffractograms of xerogels made from gel with no guests (black lines), Gel@TCPP

(red lines), Gel@Azo (green lines) and Gel@TCPP@Azo (blue lines) in water-ethanol ratio 5:5 (A) and 7:3 (B). EXTENDED DATA FIG. 4 ISOMERISATION OF AZO IN SOLUTION AND IN THE MULTICOMPONENT

GEL. UV-Visible absorption spectra of: Top. AZO 50 μM in homogeneous ethanol solution as prepared (black line) and sequential irradiation under light at 405 and 365 nm, and; Below.

Gel@TCPP@Azo in 5:5 water:ethanol under light irradiation at 405 and 365 nm. EXTENDED DATA FIG. 5 WAVELENGTH DEPENDENCE OF MOLECULAR MOTION. TIRF images of Gel@TCPP@Azo in water-ethanol 5:5

before (A-B-C-D) and after (E-F-G-H) irradiation (for a total of 8.3 minutes) with light at 405, 488, 561, 642 nm in the central region. Scale bar represents 10 μm. The difference maps below

show the areas where changes of intensity can be appreciated (note that the white and black intensities on the four maps have different intensities and do not indicate amount of change).

Some fibres in the irradiated area are darker in the difference map (so there is more porphyrin after irradiation). Those fibres are apparently above the focal plane, deeper into the sample

compared with the layer imaged. In principle, this can occur because laser intensity is higher at the slide-sample interface, then decreases as we look deeper into the sample. It is evidence

for movement of TCPP into the sample as well as to the sides of the irradiated area. EXTENDED DATA FIG. 6 RING FORMATION FROM FIBRES. Zoomed SRRF images of Gel@TCPP@Azo in water-ethanol 7:3

during irradiation at 405 nm. The frames are taken from Supplementary Video 9. Scale bar represents 2 μm, all images are to the same scale. EXTENDED DATA FIG. 7 TCPP FLUORESCENCE IN THE

GELS. The steady state fluorescence spectra (excitation wavelength 405 nm) in both 5:5 and 7:3 water:ethanol gels show (top row) that there is a quenching of the porphyrin fluorescence in

Gel@TCPP@Azo compared with Gel@TCPP for both solvent mixtures, as a result of energy transfer from the TCPP to the AZO chromophore. The middle row shows the time evolution of the same

Gel@TCPP samples under continuous irradiation at 405 nm, where a modest bleaching is observed over time for both solvent systems. The bottom row shows the evolution of the fluorescence of

Gel@TCPP@Azo under continuous irradiation, where at 5:5 water:ethanol a slight bleaching is observed (similar to Gel@TCPP), while for the 7:3 mixture an increase in fluorescence is observed,

so that after 60 minutes the intensity is actually higher than that for Gel@TCPP after the same time. EXTENDED DATA FIG. 8 ISOMERISATION OF A MAJORITY OF THE CIS-AZO ENHANCES MOTION. TIRF

micrographs from two regions at time zero with irradiation at 405 nm (top) and after the end of Supplementary Movie 13 (left) and Supplementary Video 15 (right) of sample Gel@TCPP@Azo where

AZO was enriched in the _cis_ isomer by photoisomerization prior to gel preparation. Scale bar represents 5 μm on the left hand series and 2 μm in the right hand series, all images in a

series are to the same scale. SUPPLEMENTARY INFORMATION SUPPLEMENTARY INFORMATION List of videos, Supplementary Figs. S1–S19, Tables S1–S6 and Synthetic Procedures and Characterization.

SUPPLEMENTARY VIDEO 1 TIRF video of an irradiation experiment performed on sample Gel@TCPP@Azo obtained in water:ethanol ratio 5:5. Real time 8.3 min, 20 frames per second (fps).

SUPPLEMENTARY VIDEO 2 TIRF video of an irradiation experiment performed on sample Gel@TCPP@Azo obtained in water:ethanol ratio 7:3. Real time 8.3 min, 20 fps. SUPPLEMENTARY VIDEO 3 TIRF

video of the central irradiation experiment performed on sample Gel@TCPP@Azo obtained in water:ethanol ratio 5:5. Real time 8.3 min, 20 fps. SUPPLEMENTARY VIDEO 4 TIRF video of the central

irradiation experiment performed on sample Gel@TCPP@Azo obtained in water:ethanol ratio 6:4. Real time 8.3 min, 20 fps. SUPPLEMENTARY VIDEO 5 Video of an irradiation experiment performed on

sample Gel@TCPP@Azo 5:5 using light at 405 nm. Real time 8.3 min, 20 fps. SUPPLEMENTARY VIDEO 6 Video of the irradiation experiment performed on sample Gel@TCPP@Azo 5:5 using light at 488 

nm. Real time 5 min, 10 fps. SUPPLEMENTARY VIDEO 7 Video of the irradiation experiment performed on sample Gel@TCPP@Azo 5:5 using light at 561 nm. Real time 8.3 min, 20 fps. SUPPLEMENTARY

VIDEO 8 Video of the irradiation experiment performed on sample Gel@TCPP@Azo 5:5 using light at 642 nm. Real time 8.2 min, 20 fps. SUPPLEMENTARY VIDEO 9 SRRF video of the irradiation

experiment performed on sample Gel@TCPP@Azo obtained in water:ethanol ratio 7:3. Real time 1.7 min, 10 fps. SUPPLEMENTARY VIDEO 10 TIRF video of the irradiation experiment performed on

sample Gel@TCPP obtained in water:ethanol ratio 5:5. Real time 8.3 min, 10 fps. SUPPLEMENTARY VIDEO 11 TIRF video of the irradiation experiment performed on sample Gel@TCPP obtained in

water:ethanol ratio 7:3. Real time 1.7 min, 10 fps. SUPPLEMENTARY VIDEO 12 TIRF video of the irradiation experiment performed on sample Gel@TCPP@AzoH (prepared from the sodium salt of TCPP

but with no additional base to deprotonate the AZO compound) obtained in water:ethanol ratio 5:5. Real time 8.3 min, 10 fps. SUPPLEMENTARY VIDEO 13 TIRF video of an irradiation experiment

performed on sample Gel@TCPP@Azo in 5:5 water:ethanol with a starting _trans_:_cis_ ratio of approximately 35:65 (prepared by irradiating the ethanol stock solution containing the AZO used

for the preparation of the gel at 365 nm). Real time 50 s, 5 fps. SUPPLEMENTARY VIDEO 14 TIRF video of the irradiation experiment performed on sample Gel@TCPP@Biph obtained in water:ethanol

ratio 7:3. Real time 8.3 min, 20 fps. SUPPLEMENTARY VIDEO 15 TIRF video of an irradiation experiment performed on sample Gel@TCPP@Azo in 5:5 water:ethanol with a starting _trans_:_cis_ ratio

of approximately 35:65 (prepared by irradiating the ethanol stock solution containing the AZO used for the preparation of the gel at 365 nm). Real time 120 s, 10 fps. SUPPLEMENTARY VIDEO 16

TIRF video of an irradiation experiment performed on sample Gel@TCPP@Azo obtained in water:ethanol ratio 5:5. Real time 8.3 min, 20 fps. SUPPLEMENTARY VIDEO 17 TIRF video of an irradiation

experiment performed on sample Gel@TCPP@Azo obtained in water:ethanol ratio 7:3. Real time 8.3 min, 10 fps. RIGHTS AND PERMISSIONS Reprints and permissions ABOUT THIS ARTICLE CITE THIS

ARTICLE Samperi, M., Bdiri, B., Sleet, C.D. _et al._ Light-controlled micron-scale molecular motion. _Nat. Chem._ 13, 1200–1206 (2021). https://doi.org/10.1038/s41557-021-00791-2 Download

citation * Received: 04 August 2020 * Accepted: 19 August 2021 * Published: 11 October 2021 * Issue Date: December 2021 * DOI: https://doi.org/10.1038/s41557-021-00791-2 SHARE THIS ARTICLE

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