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

doi:10.1038/s41557-022-01062-4

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 journal › Article (Academic Journal) › peer-review

65 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 language	English
Pages (from-to)	110-118
Number of pages	9
Journal	Nature Chemistry
Volume	15
Issue number	1
DOIs	https://doi.org/10.1038/s41557-022-01062-4
Publication status	Published - 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.

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© 2022, The Author(s).

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Rifaie-Graham, O., Yeow, J., Najer, A., Wang, R., Sun, R., Zhou, K., Dell, T. N., Adrianus, C., Thanapongpibul, C., Chami, M., Mann, S., de Alaniz, J. R., & Stevens, M. M. (2022). Photoswitchable gating of non-equilibrium enzymatic feedback in chemically communicating polymersome nanoreactors. Nature Chemistry, 15(1), 110-118. https://doi.org/10.1038/s41557-022-01062-4

@article{28c00203da2241e6880caf908051cbbf,

title = "Photoswitchable gating of non-equilibrium enzymatic feedback in chemically communicating polymersome nanoreactors",

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.].",

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

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{\textquoteright}s Horizon 2020 research and innovation programme under a Marie Sk{\l}odowska-Curie grant agreement (893158). J.Y. acknowledges funding from the European Union{\textquoteright}s Horizon 2020 research and innovation programme under a Marie Sk{\l}odowska-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{\textquoteright}s Horizon 2020 research and innovation programme under a Marie Sk{\l}odowska-Curie grant agreement (893158). J.Y. acknowledges funding from the European Union{\textquoteright}s Horizon 2020 research and innovation programme under a Marie Sk{\l}odowska-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: {\textcopyright} 2022, The Author(s).",

year = "2022",

month = nov,

day = "7",

doi = "10.1038/s41557-022-01062-4",

language = "English",

volume = "15",

pages = "110--118",

journal = "Nature Chemistry",

issn = "1755-4330",

publisher = "Springer Nature",

number = "1",

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TY - JOUR

T1 - Photoswitchable gating of non-equilibrium enzymatic feedback in chemically communicating polymersome nanoreactors

AU - Rifaie-Graham, Omar

AU - Yeow, Jonathan

AU - Najer, Adrian

AU - Wang, Richard

AU - Sun, Rujie

AU - Zhou, Kun

AU - Dell, Tristan N.

AU - Adrianus, Christopher

AU - Thanapongpibul, Chalaisorn

AU - Chami, Mohamed

AU - Mann, Stephen

AU - de Alaniz, Javier Read

AU - Stevens, Molly M.

N1 - 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).

PY - 2022/11/7

Y1 - 2022/11/7

N2 - 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.].

AB - 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.].

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U2 - 10.1038/s41557-022-01062-4

DO - 10.1038/s41557-022-01062-4

M3 - Article (Academic Journal)

C2 - 36344820

AN - SCOPUS:85141476799

SN - 1755-4330

VL - 15

SP - 110

EP - 118

JO - Nature Chemistry

JF - Nature Chemistry

IS - 1

ER -

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

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