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

Nature Chemistry volume 13, pages 1241–1247 (2021)Cite this article

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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 general analogue of polarimetric measurements.

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Fig. 1: Design of the enantiosensitive swimmer.
Fig. 2: Mechanism responsible for the enantiosensitive motion.
Fig. 3: Characteristic swimmer trajectories.
Fig. 4: Quantitative analysis of the swimmer speed.
Fig. 5: Monitoring of enantiomeric excess.

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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 the corresponding author on request.

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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

  1. These authors contributed equally: Serena Arnaboldi, Gerardo Salinas.

Authors and Affiliations

  1. Institut des Sciences Moléculaires, UMR 5255, University of Bordeaux, CNRS, Bordeaux INP, Pessac, France

    Serena Arnaboldi, Gerardo Salinas, Aleksandar Karajić, Patrick Garrigue & Alexander Kuhn

  2. Centre de Recherche Paul Pascal, CNRS UMR 5031, University of Bordeaux, Pessac, France

    Aleksandar Karajić, Sabrina Bichon, Sébastien Gounel & Nicolas Mano

  3. Dipartimento di Scienza e Alta Tecnologia, Università degli Studi dell’Insubria, Como, Italy

    Tiziana Benincori & Giorgia Bonetti

  4. Centro Nazionale per il Controllo e la Valutazione dei Farmaci, Istituto Superiore di Sanità, Roma, Italy

    Roberto Cirilli

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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.

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Peer review information Nature Chemistry thanks Alberto Escarpa, Xing Ma and Hong Wang for their contribution to the peer review of this work.

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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.

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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

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