Photoswitchable gating of non-equilibrium enzymatic feedback in chemically communicating polymersome nanoreactors

Omar Rifaie-Graham, Jonathan Yeow, Adrian Najer, Richard Wang, Rujie Sun, Kun Zhou, Tristan N. Dell, Christopher Adrianus, Chalaisorn Thanapongpibul, Mohamed Chami, Stephen Mann, Javier Read de Alaniz, Molly M. Stevens*

*Corresponding author for this work

Research output: Contribution to journalArticle (Academic Journal)peer-review

28 Citations (Scopus)

Abstract

The circadian rhythm generates out-of-equilibrium metabolite oscillations that are controlled by feedback loops under light/dark cycles. Here we describe a non-equilibrium nanosystem comprising a binary population of enzyme-containing polymersomes capable of light-gated chemical communication, controllable feedback and coupling to macroscopic oscillations. The populations consist of esterase-containing polymersomes functionalized with photo-responsive donor–acceptor Stenhouse adducts (DASA) and light-insensitive semipermeable urease-loaded polymersomes. The DASA–polymersome membrane becomes permeable under green light, switching on esterase activity and decreasing the pH, which in turn initiates the production of alkali in the urease-containing population. A pH-sensitive pigment that absorbs green light when protonated provides a negative feedback loop for deactivating the DASA–polymersomes. Simultaneously, increased alkali production deprotonates the pigment, reactivating esterase activity by opening the membrane gate. We utilize light-mediated fluctuations of pH to perform non-equilibrium communication between the nanoreactors and use the feedback loops to induce work as chemomechanical swelling/deswelling oscillations in a crosslinked hydrogel. We envision possible applications in artificial organelles, protocells and soft robotics. [Figure not available: see fulltext.].

Original languageEnglish
Pages (from-to)110-118
Number of pages9
JournalNature Chemistry
Volume15
Issue number1
DOIs
Publication statusPublished - 7 Nov 2022

Bibliographical note

Funding Information:
O.R.-G. acknowledges the support given by the Swiss National Science Foundation (SNSF) through an Early Postdoc. Mobility Fellowship (P2FRP2_181432) and the European Union’s Horizon 2020 research and innovation programme under a Marie Skłodowska-Curie grant agreement (893158). J.Y. acknowledges funding from the European Union’s Horizon 2020 research and innovation programme under a Marie Skłodowska-Curie grant agreement (839137). A.N. was supported from his previous SNSF Early Postdoc.Mobility Fellowship (P2BSP2_168751) and current Sir Henry Wellcome Postdoctoral Fellowship (209121_Z_17_Z) from the Wellcome Trust. R.W. acknowledges funding from The Rosetrees Trust under the Young Enterprise Fellowship agreement (A2741/M873). T.N.D. received funding under the EPSRC Doctoral Training Partnership (EP/R513052/1). C.A. acknowledges funding from the Agency for Science, Technology and Research Singapore through a National Science Scholarship. C.T. acknowledges support from a Royal Thai Government scholarship. S.M. acknowledges financial support from the European Commission (8082 H2020 PCELLS 740235). M.M.S. acknowledges support from the Royal Academy of Engineering under the Chairs in Emerging Technologies scheme (CIET2021\94). We thank P. Purhonen at the cryo-TEM measurements node at the Resource Center for Coordination of Electron Microscopy (RSEM) at KTH Royal Institute of Technology (Sweden), Y. Xu for aid with NMR spectrometers at the CFNMR Centre at Imperial College London and A. Nogiwa Valdez for extensive manuscript and data management support. We acknowledge access to facilities at the Harvey Flower Electron Microscopy Suite (Department of Materials, Imperial College London) and the Light Microscopy Facilities at the Francis Crick Institute (London, UK). The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.

Funding Information:
O.R.-G. acknowledges the support given by the Swiss National Science Foundation (SNSF) through an Early Postdoc. Mobility Fellowship (P2FRP2_181432) and the European Union’s Horizon 2020 research and innovation programme under a Marie Skłodowska-Curie grant agreement (893158). J.Y. acknowledges funding from the European Union’s Horizon 2020 research and innovation programme under a Marie Skłodowska-Curie grant agreement (839137). A.N. was supported from his previous SNSF Early Postdoc.Mobility Fellowship (P2BSP2_168751) and current Sir Henry Wellcome Postdoctoral Fellowship (209121_Z_17_Z) from the Wellcome Trust. R.W. acknowledges funding from The Rosetrees Trust under the Young Enterprise Fellowship agreement (A2741/M873). T.N.D. received funding under the EPSRC Doctoral Training Partnership (EP/R513052/1). C.A. acknowledges funding from the Agency for Science, Technology and Research Singapore through a National Science Scholarship. C.T. acknowledges support from a Royal Thai Government scholarship. S.M. acknowledges financial support from the European Commission (8082 H2020 PCELLS 740235). M.M.S. acknowledges support from the Royal Academy of Engineering under the Chairs in Emerging Technologies scheme (CIET2021\94). We thank P. Purhonen at the cryo-TEM measurements node at the Resource Center for Coordination of Electron Microscopy (RSEM) at KTH Royal Institute of Technology (Sweden), Y. Xu for aid with NMR spectrometers at the CFNMR Centre at Imperial College London and A. Nogiwa Valdez for extensive manuscript and data management support. We acknowledge access to facilities at the Harvey Flower Electron Microscopy Suite (Department of Materials, Imperial College London) and the Light Microscopy Facilities at the Francis Crick Institute (London, UK). The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.

Publisher Copyright:
© 2022, The Author(s).

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