Direct dynamic read-out of molecular chirality with autonomous enzyme-driven swimmers

ABSTRACT A key approach for designing bioinspired machines is to transfer concepts from nature to man-made structures by integrating biomolecules into artificial mechanical systems. This

strategy allows the conversion of molecular information into macroscopic action. Here, we describe the design and dynamic behaviour of hybrid bioelectrochemical swimmers that move

spontaneously at the air–water interface. Their motion is governed by the diastereomeric interactions between immobilized enantiopure oligomers and the enantiomers of a chiral probe molecule

present in solution. These dynamic bipolar systems are able to convert chiral information present at the molecular level into enantiospecific macroscopic trajectories. Depending on the

enantiomer in solution, the swimmers will move clockwise or anticlockwise; the concept can also be used for the direct visualization of the degree of enantiomeric excess by analysing the

curvature of the trajectories. Deciphering in such a straightforward way the enantiomeric ratio could be useful for biomedical applications, for the read-out of food quality or as a more

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support SIMILAR CONTENT BEING VIEWED BY OTHERS RECHARGEABLE SELF-ASSEMBLED DROPLET MICROSWIMMERS DRIVEN BY SURFACE PHASE TRANSITIONS Article 15 July 2021 VISCOELASTIC CONTROL OF

SPATIOTEMPORAL ORDER IN BACTERIAL ACTIVE MATTER Article 03 February 2021 BI-ENZYMATIC CHEMO-MECHANICAL FEEDBACK LOOP FOR CONTINUOUS SELF-SUSTAINED ACTUATION OF CONDUCTING POLYMERS Article

Open access 12 October 2023 DATA AVAILABILITY Due to an important number of different source files, the datasets generated and analysed in the frame of the current study are available from

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_Appl. Microbiol. Biotechnol._ 96, 1489–1498 (2012). Article  CAS  PubMed  PubMed Central  Google Scholar  Download references ACKNOWLEDGEMENTS The work has been funded by the European

Research Council under the European Union’s Horizon 2020 research and innovation programme (grant agreement no. 741251, European Research Council Advanced Grant ELECTRA). S.A. acknowledges

financial support from the Università degli Studi di Milano for a partial postdoc scholarship. We are also very grateful for fruitful discussions with P. Mussini. AUTHOR INFORMATION Author

notes * These authors contributed equally: Serena Arnaboldi, Gerardo Salinas. AUTHORS AND AFFILIATIONS * Institut des Sciences Moléculaires, UMR 5255, University of Bordeaux, CNRS, Bordeaux

INP, Pessac, France Serena Arnaboldi, Gerardo Salinas, Aleksandar Karajić, Patrick Garrigue & Alexander Kuhn * Centre de Recherche Paul Pascal, CNRS UMR 5031, University of Bordeaux,

Pessac, France Aleksandar Karajić, Sabrina Bichon, Sébastien Gounel & Nicolas Mano * Dipartimento di Scienza e Alta Tecnologia, Università degli Studi dell’Insubria, Como, Italy Tiziana

Benincori & Giorgia Bonetti * Centro Nazionale per il Controllo e la Valutazione dei Farmaci, Istituto Superiore di Sanità, Roma, Italy Roberto Cirilli Authors * Serena Arnaboldi View

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Scholar CONTRIBUTIONS S.A. performed the experiments and wrote and edited the manuscript. G.S. performed experiments, wrote and edited the manuscript and treated the data. A. Karajić

performed enzyme characterization and immobilization experiments. P.G. assisted with electron microscopy characterization. T.B. designed the inherently chiral monomers and edited the

manuscript. G.B. synthesized the BT2T4 molecules. R.C. separated the enantiomers by chiral HPLC. S.B. synthesized the redox polymer and tested the BOD under heterogeneous conditions. S.G.

produced, purified and tested the BOD in homogeneous solution. N.M. discussed the results and edited the manuscript. A. Kuhn proposed the research project, provided resources, designed the

experiments and edited the manuscript. CORRESPONDING AUTHOR Correspondence to Alexander Kuhn. ETHICS DECLARATIONS COMPETING INTERESTS The authors declare no competing interests. ADDITIONAL

INFORMATION PEER REVIEW INFORMATION _Nature Chemistry_ thanks Alberto Escarpa, Xing Ma and Hong Wang 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 ILLUSTRATION OF THE HYDRODYNAMIC FLOW. Illustration

of the hydrodynamic flow around the Ppy swimmer in an experiment where the swimmer is immobilized on a support. The two enantiopure oligomer-modified strips, constituting the anode, are

pointing upwards, and the enzyme covered part is oriented downwards on the image. The swimmer is placed in a 5 mM D-DOPA 0.3 M citrate/phosphate buffer (pH 5) at 22 °C containing only a

small amount of carbon beads, acting as individual tracers of the hydrodynamic flow. EXTENDED DATA FIG. 2 INFLUENCE OF IONIC STRENGTH ON THE MOTION. Z projections of the enantioselective

macroscopic motion obtained by placing swimmers with double arms ((R)-oligomer is deposited on the left arm) in three solutions of 5 mM D-DOPA at pH 5 at room temperature with different

buffer concentrations: 0.15 M (red arrow), 0.3 M (green arrow), 0.5 M (blue arrow). Black arrows indicate the initial direction of motion. The time in seconds refers to the time lapse

between two video frames, which had to be adjusted for the three experiments, as the respective speeds are very different. EXTENDED DATA FIG. 3 CHARACTERIZATION OF THE BIOELECTROCATALYTIC

REDUCTION OF OXYGEN AS A FUNCTION OF IONIC STRENGTH. Cyclic voltammograms recorded at 5 mV/s, using glassy carbon electrodes modified with redox hydrogel and BOD enzyme, in naturally aerated

buffer solutions with different ionic strength (0.15 M, 0.3 M and 0.5 M) at pH 5 and 22 °C. The hydrogel was prepared as described in the experimental procedure. The bioelectrocatalytic

reduction of oxygen is clearly visible for potentials more negative than 0.5 V, but only slightly varies as a function of the ionic strength within standard errors (≈15%). EXTENDED DATA FIG.

4 DPV ENANTIORECOGNITION TESTS FOR L-ASCORBIC ACID. DPV enantiorecognition tests carried out in a 0.3 M citrate/phosphate buffer solution at pH 5 containing 1.25 mM L-ascorbic acid (L-AA).

Measurements were performed on a glassy carbon electrode covered either with (S)-BT2T4 oligomer (red curve) or with (R)-BT2T4 oligomer (green curve). EXTENDED DATA FIG. 5 SEM MICROGRAPHS OF

THE (S)-OLIGO-BT2T4 MODIFIED PPY EXTREMITY. SEM micrographs of the (S)-oligo-BT2T4 modified Ppy extremity: (A) for the pristine swimmer, (B) same swimmer after the swimming experiments

carried out in a 0.3 M citrate/phosphate buffer solution at pH 5 at 22 °C containing 5mM L-DOPA. EXTENDED DATA FIG. 6 SEM MICROGRAPHS OF THE ENZYME HYDROGEL MODIFIED PPY EXTREMITY. SEM

micrographs of the enzyme hydrogel modified PPy extremity: (A) for the pristine swimmer, (B) same swimmer after the swimming experiments carried out in a 0.3 M citrate/phosphate buffer

solution at pH 5 at 22 °C containing 5 mM L-DOPA. EXTENDED DATA FIG. 7 EDS SIGNAL AROUND THE EMISSION PEAK OF SULPHUR. EDS signal around the emission peak of sulphur (S Kα) at the extremity

modified with the enantiopure oligomer. EXTENDED DATA FIG. 8 EDS SIGNAL FOR MEASURING THE EMISSION PEAK OF COPPER. EDS signal for measuring the emission peak of copper (Cu-Kα) of the enzyme

hydrogel modified extremity of the polypyrrole strip. The inset shows the magnification of the EDS signal of copper for the pristine swimmer (black line), and after the swimming experiments

carried out in a 0.3 M citrate/phosphate buffer solution at pH 5 at 22 °C containing 5 mM L-DOPA (red line). The decrease of this signal indicates a loss of enzyme during the swimming

experiment. EXTENDED DATA FIG. 9 EVOLUTION OF THE CURVATURE AND THE STRAIGHTNESS INDEX. Evolution of the curvature (yellow line) and the straightness index (green line) of hybrid swimmers as

a function of the enantiomeric excess. The data analysis is based on the set of experiments reported in Fig. 3, performed in triplicate. SUPPLEMENTARY INFORMATION SUPPLEMENTARY VIDEO 1

Hydrodynamic flow around a Ppy swimmer. The swimmer is placed in a 5 mM d-DOPA 0.3 M citrate/phosphate buffer (pH 5) at 22 °C containing a large concentration of 1 mm carbon beads. Video is

in real time. SUPPLEMENTARY VIDEO 2 Hydrodynamic flow around a Ppy swimmer. The swimmer is placed in a 5 mM d-DOPA 0.3 M citrate/phosphate buffer (pH 5) at 22 °C containing only one carbon

bead. Video is in real time. SUPPLEMENTARY VIDEO 3 Hydrodynamic flow around a Ppy swimmer. The swimmer is placed in a 5 mM d-DOPA 0.3 M citrate/phosphate buffer (pH 5) at 22 °C with three

carbon beads moving along one edge. Video is in real time. SUPPLEMENTARY VIDEO 4 Macroscopic enantiosensitive motion of a swimmer placed at the air–water interface of a 0.15 M

citrate/phosphate buffer (pH 5) at 22 °C containing 5 mM d-DOPA. Video is in real time. SUPPLEMENTARY VIDEO 5 Macroscopic enantiosensitive motion of a swimmer placed at the air–water

interface of a 0.5 M citrate/phosphate buffer (pH 5) at 22 °C containing 5 mM d-DOPA. Video is 16 times accelerated. SUPPLEMENTARY VIDEO 6 Macroscopic enantiosensitive clockwise motion of a

swimmer placed at the air–water interface of a 0.3 M citrate/phosphate buffer (pH 5) at 22 °C containing 5 mM d-DOPA. Video is 2 times decelerated. SUPPLEMENTARY VIDEO 7 Macroscopic

enantiosensitive anticlockwise motion of a swimmer placed at the air–water interface of a 0.3 M citrate/phosphate buffer (pH 5) at 22 °C containing 5 mM l-DOPA. Video is 2 times decelerated.

SUPPLEMENTARY VIDEO 8 Macroscopic enantiosensitive motion of two swimmers with opposite oligomer configurations placed simultaneously at the air–water interface of a 0.3 M citrate/phosphate

buffer (pH 5) at 22 °C containing 5 mM l-DOPA. Video is 2 times decelerated. SUPPLEMENTARY VIDEO 9 Macroscopic enantiosensitive motion of two swimmers with opposite oligomer configurations

placed simultaneously at the air–water interface of a 0.3 M citrate/phosphate buffer (pH 5) at 22 °C containing a racemic mixture of l- and d-DOPA with a total fixed concentration of 10 mM.

Video is 2 times decelerated. SUPPLEMENTARY VIDEO 10 Macroscopic enantiosensitive anticlockwise motion of a swimmer placed at the air–water interface of a 0.3 M citrate/phosphate buffer (pH

5) at 22 °C containing 0.25 mM l-AA. Video is 2 times decelerated. SUPPLEMENTARY VIDEO 11 Macroscopic enantiosensitive clockwise motion of a swimmer placed at the air–water interface of a

0.3 M citrate/phosphate buffer (pH 5) at 22 °C containing 0.25 mM l-AA. Video is 2 times decelerated. SUPPLEMENTARY VIDEO 12 Macroscopic enantiosensitive motion of a swimmer placed at the

surface of a bovine serum solution at 22 °C containing 10 mM l-DOPA. Video is in real time. SUPPLEMENTARY VIDEO 13 Macroscopic enantiosensitive motion of a recycled swimmer placed at the

air–water interface of a 0.3 M citrate/phosphate buffer (pH 5) containing 5 mM d-DOPA at 22 °C after immobilization of a fresh aliquot of BOD redox hydrogel on the swimmer surface. Video is

2 times decelerated. RIGHTS AND PERMISSIONS Reprints and permissions ABOUT THIS ARTICLE CITE THIS ARTICLE Arnaboldi, S., Salinas, G., Karajić, A. _et al._ Direct dynamic read-out of

molecular chirality with autonomous enzyme-driven swimmers. _Nat. Chem._ 13, 1241–1247 (2021). https://doi.org/10.1038/s41557-021-00798-9 Download citation * Received: 24 January 2021 *

Accepted: 24 August 2021 * Published: 14 October 2021 * Issue Date: December 2021 * DOI: https://doi.org/10.1038/s41557-021-00798-9 SHARE THIS ARTICLE Anyone you share the following link

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