Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Phagocytosis-inspired behaviour in synthetic protocell communities of compartmentalized colloidal objects

Abstract

The spontaneous assembly of micro-compartmentalized colloidal objects capable of controlled interactions offers a step towards rudimentary forms of collective behaviour in communities of artificial cell-like entities (synthetic protocells). Here we report a primitive form of artificial phagocytosis in a binary community of synthetic protocells in which multiple silica colloidosomes are selectively ingested by self-propelled magnetic Pickering emulsion (MPE) droplets comprising particle-free fatty acid-stabilized apertures. Engulfment of the colloidosomes enables selective delivery and release of water-soluble payloads, and can be coupled to enzyme activity within the MPE droplets. Our results highlight opportunities for the development of new materials based on consortia of colloidal objects, and provide a novel microscale engineering approach to inducing higher-order behaviour in mixed populations of synthetic protocells.

Your institute does not have access to this article

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: Design concept for phagocytosis-inspired behaviour.
Figure 2: Aperture formation in MPE droplets.
Figure 3: Engulfment of silica colloidosomes by MPE droplets.
Figure 4: Payload delivery, release and reactivity.

References

  1. Tu, Y. et al. Mimicking the cell: bio-inspired functions of supramolecular assemblies. Chem. Rev. 116, 2023–2078 (2016).

    CAS  Article  Google Scholar 

  2. Li, M., Huang, X., Tang, T.-Y. D. & Mann, S. Synthetic cellularity based on non-lipid micro-compartments and protocell models. Curr. Opin. Chem. Biol. 22, 1–11 (2014).

    Article  Google Scholar 

  3. Schoonen, L. & van Hest, J. C. M. Compartmentalization approaches in soft matter science: from nanoreactor development to organelle mimics. Adv. Mater. 28, 1109–1128 (2015).

    Article  Google Scholar 

  4. Kelly, B. T., Baret, J. C., Taly, V. & Griffiths, A. D. Miniaturizing chemistry and biology in microdroplets. Chem. Commun. 1773–1788 (2007).

  5. Mann, S. The origins of life: old problems, new chemistries. Angew. Chem. Int. Ed. Engl. 52, 155–162 (2013).

    CAS  Article  Google Scholar 

  6. 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, 1739–1745 (2011).

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  9. Pagonabarraga, I. Wetting dynamics: adsorbed colloids relax slowly. Nat. Mater. 11, 99–100 (2012).

    CAS  Article  Google Scholar 

  10. Tang, J., Quinlan, P. J. & Tam, K. C. Stimuli-responsive Pickering emulsions: recent advances and potential applications. Soft Matter 11, 3512–3529 (2015).

    CAS  Article  Google Scholar 

  11. Dinsmore, D. et al. Colloidosomes: selectively permeable capsules composed of colloidal particles. Science 298, 1006–1009 (2002).

    CAS  Article  Google Scholar 

  12. Li, Y. et al. Magnetic hydrogels and their potential biomedical applications. Adv. Funct. Mater. 23, 660–672 (2013).

    CAS  Article  Google Scholar 

  13. Wu, C., Bai, S., Ansorge-Schumacher, M. B. & Wang, D. Nanoparticle cages for enzyme catalysis in organic media. Adv. Mater. 23, 5694–5699 (2011).

    CAS  Article  Google Scholar 

  14. Akkarachaneeyakorn, K., Li, M., Davis, S. A. & Mann, S. Secretion and reversible assembly of extracellular-like matrix by enzyme-active colloidosome-based protocells. Langmuir 32, 2912–2919 (2016).

    CAS  Article  Google Scholar 

  15. Sun, S. et al. Chemical signalling and functional activation in colloidosome-based protocells. Small 12, 1920–1927 (2016).

    CAS  Article  Google Scholar 

  16. Nourian, Z. & Danelon, C. Linking genotype and phenotype in protein synthesizing liposomes with external supply of resources. ACS Synth. Biol. 2, 186–193 (2013).

    CAS  Article  Google Scholar 

  17. Martini, L. & Mansy, S. S. Cell-like systems with riboswitch controlled gene expression. Chem. Commun. 47, 10734–10736 (2011).

    CAS  Article  Google Scholar 

  18. Peters, R. J. R. W. et al. Cascade reactions in multicompartmentalized polymersomes. Angew. Chem. Int. Ed. 53, 146–150 (2014).

    CAS  Article  Google Scholar 

  19. Chandrawati, R. & Caruso, F. Biomimetic liposome- and polymersome-based multicompartmentalized assemblies. Langmuir 28, 13798–13807 (2012).

    CAS  Article  Google Scholar 

  20. Tawfik, D. S. & Griffiths, A. D. Man-made cell-like compartments for molecular evolution. Nat. Biotech. 16, 652–656 (1998).

    CAS  Article  Google Scholar 

  21. Huang, X., Patil, A. J., Li, M. & Mann, S. Design and construction of higher-order structure and function in proteinosome-based protocells. J. Am. Chem. Soc. 136, 9225–9234 (2014).

    CAS  Article  Google Scholar 

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

    Article  Google Scholar 

  23. 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  Google Scholar 

  24. Tang, T.-Y. D. et al. Fatty acid membrane assembly on coacervate microdroplets as a step towards a hybrid protocell model. Nat. Chem. 6, 527–533 (2014).

    Article  Google Scholar 

  25. Rollie, S., Mangold, M. & Sundmacher, K. Designing biological systems: systems engineering meets synthetic biology. Chem. Eng. Sci. 69, 1–29 (2012).

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  27. Schwarz-Schilling, M., Aufinger, L., Muckl, A. & Simmel, F. C. Chemical communication between bacteria and cell-free gene expression systems within linear chains of emulsion droplets. Integr. Biol. 8, 564–570 (2016).

    CAS  Article  Google Scholar 

  28. Weitz, M. et al. Diversity in the dynamical behaviour of a compartmentalized programmable biochemical oscillator. Nat. Chem. 6, 295–302 (2014).

    CAS  Article  Google Scholar 

  29. Bekki, S., Vignes-Adler, M., Nakache, E. & Adler, P. M. Solutal Marangoni effect. J. Colloid. Interface Sci. 140, 492–506 (1990).

    CAS  Article  Google Scholar 

  30. Toyota, T., Maru, N., Hanczyc, M. M., Ikegami, T. & Sugawara, T. Self-propelled oil droplets consuming “fuel” surfactant. J. Am. Chem. Soc. 131, 5012–5013 (2009).

    CAS  Article  Google Scholar 

  31. 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  Google Scholar 

  32. Ban, T., Yamagami, T., Nakata, H. & Okano, Y. pH-dependent motion of self-propelled droplets due to Marangoni effect at neutral pH. Langmuir 29, 2554–2561 (2013).

    CAS  Article  Google Scholar 

  33. Nightingale, A. M., Phillips, T. W., Bannock, J. H. & de Mello, J. C. Controlled multistep synthesis in a three-phase droplet reactor. Nat. Commun. 5, 3777 (2014).

    CAS  Article  Google Scholar 

  34. Moya-Ramírez, I., García-Román, M. & Fernández-Arteaga, A. Waste frying oil hydrolysis in a reverse micellar system. ACS Sustain. Chem. Eng. 4, 1025–1031 (2016).

    Article  Google Scholar 

Download references

Acknowledgements

We thank the European Union’s Horizon 2020 research and innovation programme for funding the work under Marie Skłodowska-Curie grant agreement, no. 656490, A. Patil for fruitful discussions, L. Powell for help with magnetite particle synthesis and MPE droplet preparation, and the Krüss Facility and Electron Microscopy Unit (School of Chemistry, University of Bristol) for assistance with contact angle/interfacial tension measurements and SEM imaging, respectively.

Author information

Authors and Affiliations

Authors

Contributions

L.R.-A., M.L. and S.M. conceived the experiments; L.R.-A. performed the experiments; L.R.-A. and M.L. undertook the data analysis; L.R.-A., M.L. and S.M. wrote the manuscript.

Corresponding author

Correspondence to Stephen Mann.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Information (PDF 763 kb)

Supplementary Information

Supplementary movie 1 (MP4 28268 kb)

Supplementary Information

Supplementary movie 2 (MP4 29554 kb)

Supplementary Information

Supplementary movie 3 (MP4 26446 kb)

Supplementary Information

Supplementary movie 4 (MP4 22374 kb)

Supplementary Information

Supplementary movie 5 (MP4 56307 kb)

Supplementary Information

Supplementary movie 6 (MP4 40402 kb)

Supplementary Information

Supplementary movie 7 (MP4 30410 kb)

Supplementary Information

Supplementary movie 8 (MP4 17620 kb)

Supplementary Information

Supplementary movie 9 (MP4 11440 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Rodríguez-Arco, L., Li, M. & Mann, S. Phagocytosis-inspired behaviour in synthetic protocell communities of compartmentalized colloidal objects. Nature Mater 16, 857–863 (2017). https://doi.org/10.1038/nmat4916

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nmat4916

Further reading

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing