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Enzyme-powered motility in buoyant organoclay/DNA protocells

Nature Chemistry volume 10, pages 1154–1163 (2018)Cite this article

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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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References

  1. Jarrell, K. F. & McBride, M. J. The surprisingly diverse ways that prokaryotes move. Nat. Rev. Microbiol. 6, 466–476 (2008).

    Article  CAS  PubMed  Google Scholar 

  2. Herold, C., Leduc, C., Stock, R., Diez, S. & Schwille, P. Long-range transport of giant vesicles along microtubule networks. ChemPhysChem 13, 1001–1006 (2012).

    Article  CAS  PubMed  Google Scholar 

  3. Bottier, C. et al. Active transport of oil droplets along oriented microtubules by kinesin molecular motors. Lab Chip 9, 1694–1700 (2009).

    Article  CAS  PubMed  Google Scholar 

  4. Sánchez, S., Soler, L. & Katuri, J. Chemically powered micro- and nanomotors. Angew. Chem. Int. Ed. 54, 1414–1444 (2015).

    Article  CAS  Google Scholar 

  5. Guix, M., Mayorga-Martinez, C. C. & Merkoçi, A. Nano/micromotors in (bio)chemical science applications. Chem. Rev. 114, 6285–6322 (2014).

    Article  CAS  PubMed  Google Scholar 

  6. Loget, G. & Kuhn, A. Electric field-induced chemical locomotion of conducting objects. Nat. Commun. 2, 535 (2011).

    Article  CAS  PubMed  Google Scholar 

  7. Dreyfus, R. et al. Microscopic artificial swimmers. Nature 437, 862–865 (2005).

    Article  CAS  PubMed  Google Scholar 

  8. Ghosh, A. & Fischer, P. Controlled propulsion of artificial magnetic nanostructured propellers. Nano Lett. 9, 2243–2245 (2009).

    Article  CAS  PubMed  Google Scholar 

  9. Ibele, M., Mallouk, T. E. & Sen, A. Schooling behavior of light-powered autonomous micromotors in water. Angew. Chem. Int. Ed. 48, 3308–3312 (2009).

    Article  CAS  Google Scholar 

  10. Hong, Y., Diaz, M., Córdova-Figueroa, U. M. & Sen, A. Light-driven titanium-dioxide-based reversible microfireworks and micromotor/micropump systems. Adv. Funct. Mater. 20, 1568–1576 (2010).

    Article  CAS  Google Scholar 

  11. Wang, W. et al. Acoustic propulsion of nanorod motors inside living cells. Angew. Chem. 126, 3265–3268 (2014).

    Article  Google Scholar 

  12. Wang, W., Castro, L. A., Hoyos, M. & Mallouk, T. E. Autonomous motion of metallic microrods propelled by ultrasound. ACS Nano 6, 6122–6132 (2012).

    Article  CAS  PubMed  Google Scholar 

  13. Paxton, W.F. et al. Catalytic nanomotors: autonomous movement of striped nanorods. J. Am Chem. Soc. 126, 13424–13431 (2004).

    Article  CAS  PubMed  Google Scholar 

  14. Howse, J. R. et al. Self-motile colloidal particles: from directed propulsion to random walk. Phys. Rev. Lett. 99, 048102 (2007).

    Article  CAS  PubMed  Google Scholar 

  15. Vicario, J. et al. Catalytic molecular motors: fuelling autonomous movement by a surface bound synthetic manganese catalase. Chem. Commun. 3936–3938 (2005).

  16. Pantarotto, D., Browne, W. R. & Feringa, B. L. Autonomous propulsion of carbon nanotubes powered by a multienzyme ensemble. Chem. Commun. 1533–1535 (2008).

  17. Schattling, P., Thingholm, B. & Städler, B. Enhanced diffusion of glucose-fueled Janus particles. Chem. Mater. 27, 7412–7418 (2015).

    Article  CAS  Google Scholar 

  18. Solovev, A. A., Smith, E. J., Bof’ Bufon, C. C., Sanchez, S. & Schmidt, O. G. Light-controlled propulsion of catalytic microengines. Angew. Chem. Int. Ed. 50, 10875–10878 (2011).

    Article  CAS  Google Scholar 

  19. Baraban, L. et al. Catalytic Janus motors on microfluidic chip: deterministic motion for targeted cargo delivery. ACS Nano 6, 3383–3389 (2012).

    Article  CAS  PubMed  Google Scholar 

  20. Xu, T. et al. Reversible swarming and separation of self-propelled chemically powered nanomotors under acoustic fields. J. Am. Chem. Soc. 137, 2163–2166 (2015).

    Article  CAS  PubMed  Google Scholar 

  21. Krishna Kumar, R., Yu, X., Patil, A. J., Li, M. & Mann, S. Cytoskeletal-like supramolecular assembly and nanoparticle-based motors in a model protocell. Angew. Chem. Int. Ed. 50, 9343–9347 (2011).

    Article  CAS  Google Scholar 

  22. Wilson, D. A., Nolte, R. J. M. & van Hest, J. C. M. Autonomous movement of platinum-loaded stomatocytes. Nat. Chem. 4, 268–274 (2012).

    Article  CAS  PubMed  Google Scholar 

  23. Peng, F., Tu, Y., van Hest, J. C. M. & Wilson, D. A. Self-guided supramolecular cargo-loaded nanomotors with chemotactic behavior towards cells. Angew. Chem. Int. Ed. 54, 11662–11665 (2015).

    Article  CAS  Google Scholar 

  24. Peng, F., Tu, Y., Men, Y., van Hest, J. C. M. & Wilson, D. A. Supramolecular adaptive nanomotors with magnetotaxis behavior. Adv. Mater. 29, 1604996 (2017).

    Article  CAS  Google Scholar 

  25. Lu, A. X. et al. Catalytic propulsion and magnetic steering of soft, patchy microcapsules: ability to pick-up and drop-off microscale cargo. ACS Appl. Mater. Interfaces 8, 15676–15683 (2016).

    Google Scholar 

  26. Nijemeisland, M., Abdelmohsen, L. K. E. A., Huck, W. T. S., Wilson, D. A. & van Hest, J. C. M. A compartmentalized out-of-equilibrium enzymatic reaction network for sustained autonomous movement. ACS Cent. Sci. 2, 843–849 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Abdelmohsen, L. K. E. A. et al. Dynamic loading and unloading of proteins in polymeric stomatocytes: formation of an enzyme-loaded supramolecular nanomotor. ACS Nano 10, 2652–2660 (2016).

    Article  CAS  PubMed  Google Scholar 

  28. Ma, X. et al. Enzyme-powered hollow mesoporous Janus nanomotors. Nano Lett. 15, 7043–7050 (2015).

    Article  CAS  PubMed  Google Scholar 

  29. Wu, Y., Lin, X., Wu, Z., Möhwald, H. & He, Q. Self-propelled polymer multilayer Janus capsules for effective drug delivery and light-triggered release. ACS Appl. Mater. Interfaces 6, 10476–10481 (2014).

    Google Scholar 

  30. Ma, X., Wang, X., Hahn, K. & Sánchez, S. Motion control of urea-powered biocompatible hollow microcapsules. ACS Nano 10, 3597–3605 (2016).

    Article  CAS  PubMed  Google Scholar 

  31. Ma, X., Hortelão, A. C., Patiño, T. & Sánchez, S. Enzyme catalysis to power micro/nanomachines. ACS Nano 10, 9111–9122 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Ortiz-Rivera, I., Courtney, T. M. & Sen, A. Enzyme micropump-based inhibitor assays. Adv. Funct. Mater. 26, 2135–2142 (2016).

    Article  CAS  Google Scholar 

  33. Lach, S. et al. Tactic, reactive, and functional droplets outside of equilibrium. Chem. Soc. Rev. 65, 1392–1399 (2016).

    Google Scholar 

  34. Hanczyc, M. M., Toyota, T., Ikegami, T., Packard, N. & Sugawara, T. Fatty acid chemistry at the oil−water interface: self-propelled oil droplets. J. Am. Chem. Soc. 129, 9386–9391 (2007).

    Article  CAS  PubMed  Google Scholar 

  35. Ichimura, K., Oh, S.-K. & Nakagawa, M. Light-driven motion of liquids on a photoresponsive surface. Science 288, 1624–1626 (2000).

    Article  CAS  PubMed  Google Scholar 

  36. Tang, X. et al. Photochemically induced motion of liquid metal marbles. Appl. Phys. Lett. 103, 174104 (2013).

    Article  CAS  Google Scholar 

  37. Qiao, Y., Li, M., Booth, R. & Mann, S. Predatory behaviour in synthetic protocell communities. Nat. Chem. 9, 110–119 (2017).

    Article  CAS  PubMed  Google Scholar 

  38. Rodriguez-Arco, L., Li, M. & Mann, S. Phagocytosis-inspired behaviour in synthetic protocell communities of compartmentalized colloidal objects. Nat. Mater. 16, 857–863 (2017).

    Article  CAS  PubMed  Google Scholar 

  39. Pfeifer, F. Distribution, formation and regulation of gas vesicles. Nat. Rev. Microbiol. 10, 705–715 (2012).

    Article  CAS  PubMed  Google Scholar 

  40. Enríquez, O. R. et al. Growing bubbles in a slightly supersaturated liquid solution. Rev. Sci. Instrum. 84, 065111 (2013).

    Article  CAS  PubMed  Google Scholar 

  41. Li, M., Green, D. C., Anderson, J. L. R., Binks, B. P. & Mann, S. In vitro gene expression and enzyme catalysis in bio-inorganic protocells. Chem. Sci. 2, 1739 (2011).

    Article  CAS  Google Scholar 

  42. Li, M., Harbron, R., Weaver, J., Binks, B. & Mann, S. Electrostatically gated membrane permeability in inorganic protocells. Nat. Chem. 5, 529–536 (2013).

    Article  CAS  PubMed  Google Scholar 

  43. Huang, X. et al. Interfacial assembly of protein–polymer nano-conjugates into stimulus-responsive biomimetic protocells. Nat. Commun. 4, 2239 (2013).

    Article  CAS  PubMed  Google Scholar 

  44. Koga, S., Williams, D. S., Perriman, A. W. & Mann, S. Peptide–nucleotide microdroplets as a step towards a membrane-free protocell model. Nat. Chem. 3, 720–724 (2011).

    Article  CAS  PubMed  Google Scholar 

  45. Szostak, J. W., Bartel, D. P. & Luisi, P. L. Synthesizing life. Nature 409, 387–390 (2001).

    Article  CAS  PubMed  Google Scholar 

  46. Walde, P. & Ichikawa, S. Enzymes inside lipid vesicles: preparation, reactivity and applications. Biomol. Eng. 18, 143–177 (2001).

    Article  CAS  PubMed  Google Scholar 

  47. Datta, K. K. R., Achari, a & Eswaramoorthy, M. Aminoclay: a functional layered material with multifaceted applications. J. Mater. Chem. A 1, 6707 (2013).

    Article  CAS  Google Scholar 

  48. Kumar, R. K., Li, M., Olof, S. N., Patil, A. J. & Mann, S. Artificial cytoskeletal structures within enzymatically active bio-inorganic protocells. Small 9, 357–362 (2013).

    Article  CAS  PubMed  Google Scholar 

  49. Li, M., Huang, X. & Mann, S. Spontaneous growth and division in self-reproducing inorganic colloidosomes. Small 10, 3291–3298 (2014).

    Article  CAS  PubMed  Google Scholar 

  50. Tang, T.-Y. D., van Swaay, D., deMello, A., Ross Anderson, J. L. & Mann, S. In vitro gene expression within membrane-free coacervate protocells. Chem. Commun. 51, 11429–11432 (2015).

    Article  Google Scholar 

  51. Bozzano, G. & Dente, M. Shape and terminal velocity of single bubble motion: a novel approach. Comput. Chem. Eng. 25, 571–576 (2001).

    Article  CAS  Google Scholar 

  52. Klein, J., Stock, J. & Vorlop, K.-D. Pore size and properties of spherical Ca-alginate biocatalysts. Eur. J. Appl. Microbiol. Biotechnol. 18, 86–91 (1983).

    Article  CAS  Google Scholar 

  53. Patil, A. J., Muthusamy, E. & Mann, S. Fabrication of functional protein–organoclay lamellar nanocomposites by biomolecule-induced assembly of exfoliated aminopropyl-functionalized magnesium phyllosilicates. J. Mater. Chem. 15, 3838–3843 (2005).

    Article  CAS  Google Scholar 

  54. Burkett, S. L. & Press, A. & Mann S. Synthesis, characterization, and reactivity of layered inorganic−organic nanocomposites based on 2:1 trioctahedral phyllosilicates. Chem. Mater. 9, 1071–1073 (1997).

    Article  CAS  Google Scholar 

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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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Authors and Affiliations

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

    B. V. V. S. Pavan Kumar, Avinash J. Patil & Stephen Mann

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  1. B. V. V. S. Pavan Kumar
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Contributions

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.

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Correspondence to Avinash J. Patil or Stephen Mann.

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The authors declare no competing interests.

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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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