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Enzyme-powered motility in buoyant organoclay/DNA protocells


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.


  1. 1.

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

    CAS  Article  PubMed  Google Scholar 

  2. 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).

    CAS  Article  PubMed  Google Scholar 

  3. 3.

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

    CAS  Article  PubMed  Google Scholar 

  4. 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. 5.

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

    CAS  Article  PubMed  Google Scholar 

  6. 6.

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

    Article  CAS  PubMed  Google Scholar 

  7. 7.

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

    CAS  Article  PubMed  Google Scholar 

  8. 8.

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

    CAS  Article  PubMed  Google Scholar 

  9. 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).

    CAS  Article  Google Scholar 

  10. 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).

    CAS  Article  Google Scholar 

  11. 11.

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

    Article  Google Scholar 

  12. 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).

    CAS  Article  PubMed  Google Scholar 

  13. 13.

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

    CAS  Article  PubMed  Google Scholar 

  14. 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. 15.

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

  16. 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. 17.

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

    CAS  Article  Google Scholar 

  18. 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).

    CAS  Article  Google Scholar 

  19. 19.

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

    CAS  Article  PubMed  Google Scholar 

  20. 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).

    CAS  Article  PubMed  Google Scholar 

  21. 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).

    CAS  Article  Google Scholar 

  22. 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).

    CAS  Article  PubMed  Google Scholar 

  23. 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).

    CAS  Article  Google Scholar 

  24. 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. 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. 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).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  27. 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).

    CAS  Article  PubMed  Google Scholar 

  28. 28.

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

    Article  CAS  PubMed  Google Scholar 

  29. 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. 30.

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

    CAS  Article  PubMed  Google Scholar 

  31. 31.

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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  32. 32.

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

    CAS  Article  Google Scholar 

  33. 33.

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

    Google Scholar 

  34. 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).

    CAS  Article  PubMed  Google Scholar 

  35. 35.

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

    CAS  Article  PubMed  Google Scholar 

  36. 36.

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

    Article  CAS  Google Scholar 

  37. 37.

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

    CAS  Article  PubMed  Google Scholar 

  38. 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).

    CAS  Article  PubMed  Google Scholar 

  39. 39.

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

    CAS  Article  PubMed  Google Scholar 

  40. 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. 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).

    CAS  Article  Google Scholar 

  42. 42.

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

    CAS  Article  PubMed  Google Scholar 

  43. 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. 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).

    CAS  Article  PubMed  Google Scholar 

  45. 45.

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

    CAS  Article  PubMed  Google Scholar 

  46. 46.

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

    CAS  Article  PubMed  Google Scholar 

  47. 47.

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

    CAS  Article  Google Scholar 

  48. 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).

    CAS  Article  PubMed  Google Scholar 

  49. 49.

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

    CAS  Article  PubMed  Google Scholar 

  50. 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. 51.

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

    CAS  Article  Google Scholar 

  52. 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).

    CAS  Article  Google Scholar 

  53. 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).

    CAS  Article  Google Scholar 

  54. 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).

    CAS  Article  Google Scholar 

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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.

Author information




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).

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