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Chemical-mediated translocation in protocell-based microactuators

Nature Chemistry volume 13, pages 868–879 (2021)Cite this article

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Abstract

Artificial cell-like communities participate in diverse modes of chemical interaction but exhibit minimal interfacing with their local environment. Here we develop an interactive microsystem based on the immobilization of a population of enzyme-active semipermeable proteinosomes within a helical hydrogel filament to implement signal-induced movement. We attach large single-polynucleotide/peptide microcapsules at one or both ends of the helical protocell filament to produce free-standing soft microactuators that sense and process chemical signals to perform mechanical work. Different modes of translocation are achieved by synergistic or antagonistic enzyme reactions located within the helical connector or inside the attached microcapsule loads. Mounting the microactuators on a ratchet-like surface produces a directional push–pull movement. Our methodology opens up a route to protocell-based chemical systems capable of utilizing mechanical work and provides a step towards the engineering of soft microscale objects with increased levels of operational autonomy.

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Fig. 1: Microfluidic preparation of protocell-embedded helical hydrogel filaments.
Fig. 2: Protocell-mediated elastic behaviour.
Fig. 3: Protocell-mediated energy release and helical hydrogel filament elongation.
Fig. 4: Protocell-induced contraction of extended helical hydrogel filaments.
Fig. 5: Protocell-mediated reversible contraction of helical hydrogel filaments.
Fig. 6: Enzyme-mediated translocation in protocell-based microactuators.
Fig. 7: Endogenous transmission in protocell-based microactuators.
Fig. 8: Antagonistic modes of transmission in protocell-based microactuators.

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Data availability

All data supporting the results and conclusions are available within this paper and the Supplementary Information. Copies of the raw data can be obtained via the link: https://figshare.com/articles/figure/NCHEM-20071608A_zip/14331317. Source data are provided with this paper.

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Acknowledgements

We thank the European Commission for financial support (8082 H2020 PCELLS 740235); the Wolfson Bioimaging Facility and the Chemical Imaging Facility for help with characterization; A. McAleer and J. Liu for assistance with ICP-OES measurements; C. Xu for help with preparing ultrasmall proteinosomes; I. Myrgorodska and Z. Yin for providing BSA nanoconjugates; R. Moreno Tortolero for assistance with developing the microforce measurement system; P. Peschke for help with recording microfocal images; and Z. Shen for butterfly wing samples and suggesting their use as a ratchet-like surface.

Author information

Authors and Affiliations

  1. Centre for Protolife Research and Centre for Organized Matter Chemistry, School of Chemistry, University of Bristol, Bristol, UK

    Ning Gao, Mei Li, Liangfei Tian, Avinash J. Patil, B. V. V. S. Pavan Kumar & Stephen Mann

  2. Max Planck-Bristol Centre for Minimal Biology, School of Chemistry, University of Bristol, Bristol, UK

    Ning Gao & Stephen Mann

  3. School of Materials Science and Engineering, Shanghai Jiao Tong University, Shanghai, P. R. China

    Mei Li & Stephen Mann

  4. Key Laboratory of Biomedical Engineering of Ministry of Education, Zhejiang Provincial Key Laboratory of Cardio-Cerebral Vascular Detection Technology and Medicinal Effectiveness Appraisal, Department of Biomedical Engineering, Zhejiang University, Hangzhou, P. R. China

    Liangfei Tian

  5. Department of Chemistry, Indian Institute of Technology Roorkee, Roorkee, India

    B. V. V. S. Pavan Kumar

Authors
  1. Ning Gao
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Contributions

N.G., M.L. and S.M. conceived the experiments. N.G. undertook the experiments. L.T. assisted with constructing the bilateral microactuators. A.J.P and B.V.V.S.P.K. prepared DNA/protamine microcapsules. N.G., M.L., L.T. and S.M. undertook the data analysis. L.T. contributed to the preparation of the manuscript. N.G., M.L. and S.M. wrote the manuscript. All authors commented on the manuscript.

Corresponding authors

Correspondence to Mei Li or Stephen Mann.

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The authors declare no competing interests.

Additional information

Peer review information Nature Chemistry thanks Esther Amstad, Oliver Castell and the other, anonymous, reviewer(s) 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.

Supplementary information

Supplementary Information

Supplementary Materials and Methods, description of the videos and Figs. 1–33.

Supplementary Video 1

Confocal laser scanning microscopy video showing morphology of the ultrasmall FITC-labelled proteinosomes.

Supplementary Video 2

Fluorescence microscopy video showing formation of a protocell/hydrogel helical filament in a glass capillary microfluidic device.

Supplementary Video 3

Fluorescence microscopy video showing the 3D structure of a protocell/hydrogel helical filament.

Supplementary Video 4

Optical microscopy video showing protocell-mediated energy release in a single helical filament of hydrogel-immobilized (3 wt% sodium alginate; 2 wt% CaCl2) urease-containing proteinosomes after addition of urea (3 ml, 60 mM).

Supplementary Video 5

Optical microscopy video showing use of a protocell/hydrogel helical filament as a microactuator.

Supplementary Video 6

Optical microscopy video showing synergistic mode of endogenous transmission in an integrated free-standing protocell-based microactuator.

Supplementary Video 7

Optical microscopy video showing translocation of a single urease-containing DNA/protamine microcapsule (urease, 10 mg ml−1) attached to one end of a helical filament microactuator filament (3 wt% Na alginate, 2 wt% CaCl2) after addition of urea (3 ml, 5 mM).

Supplementary Video 8

Optical microscopy video showing consecutive pitch extension and contraction of a protocell-based microactuator as the pitch is extended and contracted respectively by the influx of urea (5 mM, 2 ml h−1) or CaCl2 (1 wt%, 2 ml h−1).

Source data

Source Data Fig. 1

Statistical Source Data for Fig. 1h.

Source Data Fig. 2

Statistical Source Data for Fig. 2b,c.

Source Data Fig. 3

Statistical Source Data for Fig. 3c–h.

Source Data Fig. 4

Statistical Source Data for Fig. 4c,d,f–i.

Source Data Fig. 5

Statistical Source Data for Fig. 5c.

Source Data Fig. 6

Statistical Source Data for Fig. 6b,h.

Source Data Fig. 7

Statistical Source Data for Fig. 7c,i.

Source Data Fig. 8

Statistical Source Data for Fig. 8d,g,h.

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Gao, N., Li, M., Tian, L. et al. Chemical-mediated translocation in protocell-based microactuators. Nat. Chem. 13, 868–879 (2021). https://doi.org/10.1038/s41557-021-00728-9

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