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Enzyme-powered motility in buoyant organoclay/DNA protocells

Abstract

Reconstitution and simulation of cellular motility in microcompartmentalized colloidal objects have important implications for microcapsule-based remote sensing, environmentally induced signalling between artificial cell-like entities and programming spatial migration in synthetic protocell consortia. Here we describe the design and construction of catalase-containing organoclay/DNA semipermeable microcapsules, which in the presence of hydrogen peroxide exhibit enzyme-powered oxygen gas bubble-dependent buoyancy. We determine the optimum conditions for single and/or multiple bubble generation per microcapsule, monitor the protocell velocities and resilience, and use remote magnetic guidance to establish reversible changes in the buoyancy. Co-encapsulation of catalase and glucose oxidase is exploited to establish a spatiotemporal response to antagonistic bubble generation and depletion to produce protocells capable of sustained oscillatory vertical movement. We demonstrate that the motility of the microcapsules can be used for the flotation of macroscopic objects, self-sorting of mixed protocell communities and the delivery of a biocatalyst from an inert to chemically active environment. These results highlight new opportunities to constructing programmable microcompartmentalized colloids with buoyancy-derived motility.

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Fig. 1: Fabrication of organoclay/DNA microcapsules.
Fig. 2: General properties of organoclay/DNA microcapsules.
Fig. 3: Buoyant motility in organoclay/DNA microcapsules.
Fig. 4: Nucleation and growth of oxygen microbubbles in organoclay/DNA microcapsules.
Fig. 5: Oscillatory motion of organoclay/DNA microcapsules.
Fig. 6: Properties of motile populations of organoclay/DNA microcapsules.

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Acknowledgements

We thank the EPSRC, ERC Advanced Grant Scheme, BrisSynBio, Marie-Curie Individual Fellowship (B.V.V.S.P.K) and University of Bristol (A.J.P.) for financial support, D. Tarling for assistance with the fabrication of specifically designed glassware, L. Tian for useful discussions and M. Li, D. S. Williams and R. Krishna Kumar for assistance with the preliminary experiments.

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B.V.V.S.P.K., A.J.P. and S.M. conceived the experiments; B.V.V.S.P.K. and A.J.P. performed the experiments; B.V.V.S.P.K., A.J.P. and S.M. undertook data analysis; B.V.V.S.P.K., A.J.P. and S.M. wrote the manuscript.

Corresponding authors

Correspondence to Avinash J. Patil or Stephen Mann.

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Supplementary information

Supplementary Information

Supplementary Files, Methods and Figures

Supplementary Video 1

Buoyancy-induced motility in catalase-containing organoclay/DNA microcapsules

Supplementary Video 2

Growth of oxygen microbubbles with organoclay/DNA microcapsules

Supplementary Video 3

Growth of bubble until the rupture of organoclay/DNA microcapsule and subsequent release

Supplementary Video 4

Vertical up-down oscillations of organoclay/DNA capsules

Supplementary Video 5

Oscillatory movement of organoclay/DNA microcapsules mediated by remote magnetic guidance

Supplementary Video 6

Flotation of macroscopic objects

Supplementary Video 7

Segregation of mixed protocell communities

Supplementary Video 8

Transfer between different chemical environments

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Kumar, B.V.V.S.P., Patil, A.J. & Mann, S. Enzyme-powered motility in buoyant organoclay/DNA protocells. Nature Chem 10, 1154–1163 (2018). https://doi.org/10.1038/s41557-018-0119-3

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