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Title: Light‐Gated Synthetic Protocells for Plasmon‐Enhanced Chemiosmotic Gradient Generation and ATP Synthesis

Abstract

Abstract Herein, we present a light‐gated protocell model made of plasmonic colloidal capsules (CCs) assembled with bacteriorhodopsin for converting solar energy into electrochemical gradients to drive the synthesis of energy‐storage molecules. This synthetic protocell incorporated an important intrinsic property of noble metal colloidal particles, namely, plasmonic resonance. In particular, the near‐field coupling between adjacent metal nanoparticles gave rise to strongly localized electric fields and resulted in a broad absorption in the whole visible spectra, which in turn promoted the flux of photons to bacteriorhodopsin and accelerated the proton pumping kinetics. The cell‐like potential of this design was further demonstrated by leveraging the outward pumped protons as “chemical signals” for triggering ATP biosynthesis in a coexistent synthetic protocell population. Hereby, we lay the ground work for the engineering of colloidal supraparticle‐based synthetic protocells with higher‐order functionalities.

Authors:
 [1];  [1]; ORCiD logo [1];  [2]; ORCiD logo [1];  [2]; ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [3]; ORCiD logo [1]
  1. Center for Nanoscale Materials Argonne National Laboratory Argonne IL 60439 USA
  2. Applied Materials Division Argonne National Laboratory Argonne IL 60439 USA
  3. Biosciences Division Argonne National Laboratory Argonne IL 60439 USA
Publication Date:
Sponsoring Org.:
USDOE
OSTI Identifier:
1495274
Grant/Contract Number:  
AC02- 06CH11357
Resource Type:
Publisher's Accepted Manuscript
Journal Name:
Angewandte Chemie
Additional Journal Information:
Journal Name: Angewandte Chemie Journal Volume: 131 Journal Issue: 15; Journal ID: ISSN 0044-8249
Publisher:
Wiley Blackwell (John Wiley & Sons)
Country of Publication:
Germany
Language:
English

Citation Formats

Chen, Zhaowei, De Queiros Silveira, Gleiciani, Ma, Xuedan, Xie, Yunsong, Wu, Yimin A., Barry, Edward, Rajh, Tijana, Fry, H. Christopher, Laible, Philip D., and Rozhkova, Elena A. Light‐Gated Synthetic Protocells for Plasmon‐Enhanced Chemiosmotic Gradient Generation and ATP Synthesis. Germany: N. p., 2019. Web. doi:10.1002/ange.201813963.
Chen, Zhaowei, De Queiros Silveira, Gleiciani, Ma, Xuedan, Xie, Yunsong, Wu, Yimin A., Barry, Edward, Rajh, Tijana, Fry, H. Christopher, Laible, Philip D., & Rozhkova, Elena A. Light‐Gated Synthetic Protocells for Plasmon‐Enhanced Chemiosmotic Gradient Generation and ATP Synthesis. Germany. https://doi.org/10.1002/ange.201813963
Chen, Zhaowei, De Queiros Silveira, Gleiciani, Ma, Xuedan, Xie, Yunsong, Wu, Yimin A., Barry, Edward, Rajh, Tijana, Fry, H. Christopher, Laible, Philip D., and Rozhkova, Elena A. Wed . "Light‐Gated Synthetic Protocells for Plasmon‐Enhanced Chemiosmotic Gradient Generation and ATP Synthesis". Germany. https://doi.org/10.1002/ange.201813963.
@article{osti_1495274,
title = {Light‐Gated Synthetic Protocells for Plasmon‐Enhanced Chemiosmotic Gradient Generation and ATP Synthesis},
author = {Chen, Zhaowei and De Queiros Silveira, Gleiciani and Ma, Xuedan and Xie, Yunsong and Wu, Yimin A. and Barry, Edward and Rajh, Tijana and Fry, H. Christopher and Laible, Philip D. and Rozhkova, Elena A.},
abstractNote = {Abstract Herein, we present a light‐gated protocell model made of plasmonic colloidal capsules (CCs) assembled with bacteriorhodopsin for converting solar energy into electrochemical gradients to drive the synthesis of energy‐storage molecules. This synthetic protocell incorporated an important intrinsic property of noble metal colloidal particles, namely, plasmonic resonance. In particular, the near‐field coupling between adjacent metal nanoparticles gave rise to strongly localized electric fields and resulted in a broad absorption in the whole visible spectra, which in turn promoted the flux of photons to bacteriorhodopsin and accelerated the proton pumping kinetics. The cell‐like potential of this design was further demonstrated by leveraging the outward pumped protons as “chemical signals” for triggering ATP biosynthesis in a coexistent synthetic protocell population. Hereby, we lay the ground work for the engineering of colloidal supraparticle‐based synthetic protocells with higher‐order functionalities.},
doi = {10.1002/ange.201813963},
journal = {Angewandte Chemie},
number = 15,
volume = 131,
place = {Germany},
year = {Wed Feb 20 00:00:00 EST 2019},
month = {Wed Feb 20 00:00:00 EST 2019}
}

Works referenced in this record:

Artificial Cells: Synthetic Compartments with Life-like Functionality and Adaptivity
journal, January 2017


Der schmale Pfad tief in die Vergangenheit: auf der Suche nach der Chemie der Anfänge des Lebens
journal, July 2017


Individual Surface-Engineered Microorganisms as Robust Pickering Interfacial Biocatalysts for Resistance-Minimized Phase-Transfer Bioconversion
journal, February 2015

  • Chen, Zhaowei; Ji, Haiwei; Zhao, Chuanqi
  • Angewandte Chemie International Edition, Vol. 54, Issue 16
  • DOI: 10.1002/anie.201412049

Plasmonic Field Enhancement of the Bacteriorhodopsin Photocurrent during Its Proton Pump Photocycle
journal, June 2010

  • Yen, Chun-Wan; Chu, Li-Kang; El-Sayed, Mostafa A.
  • Journal of the American Chemical Society, Vol. 132, Issue 21
  • DOI: 10.1021/ja101301u

Bio-Functional Mesolamellar Nanocomposites Based on Inorganic/Polymer Intercalation in Purple Membrane (Bacteriorhodopsin) Films
journal, September 2007

  • Bromley, K. M.; Patil, A. J.; Seddon, A. M.
  • Advanced Materials, Vol. 19, Issue 18
  • DOI: 10.1002/adma.200602250

Multifunctional Porous Microspheres Based on Peptide-Porphyrin Hierarchical Co-Assembly
journal, January 2014

  • Zou, Qianli; Zhang, Lu; Yan, Xuehai
  • Angewandte Chemie International Edition, Vol. 53, Issue 9
  • DOI: 10.1002/anie.201308792

Nanoparticle Assembly and Transport at Liquid-Liquid Interfaces
journal, January 2003


Hydrothermal vents and the origin of life
journal, September 2008

  • Martin, William; Baross, John; Kelley, Deborah
  • Nature Reviews Microbiology, Vol. 6, Issue 11
  • DOI: 10.1038/nrmicro1991

Bacteriorhodopsin as a Photochromic Retinal Protein for Optical Memories
journal, May 2000


Synthetic beta cells for fusion-mediated dynamic insulin secretion
journal, October 2017

  • Chen, Zhaowei; Wang, Jinqiang; Sun, Wujin
  • Nature Chemical Biology, Vol. 14, Issue 1
  • DOI: 10.1038/nchembio.2511

Electrostatically gated membrane permeability in inorganic protocells
journal, May 2013

  • Li, Mei; Harbron, Rachel L.; Weaver, Jonathan V. M.
  • Nature Chemistry, Vol. 5, Issue 6
  • DOI: 10.1038/nchem.1644

Cell-Free Synthetic Biology Chassis for Nanocatalytic Photon-to-Hydrogen Conversion
journal, June 2017


Dependence of Fluorescence Intensity on the Spectral Overlap between Fluorophores and Plasmon Resonant Single Silver Nanoparticles
journal, March 2007

  • Chen, Yeechi; Munechika, Keiko; Ginger, David S.
  • Nano Letters, Vol. 7, Issue 3
  • DOI: 10.1021/nl062795z

The Narrow Road to the Deep Past: In Search of the Chemistry of the Origin of Life
journal, July 2017


A Membrane-Reconstituted Multisubunit Functional Proton Pump on Mesoporous Silica Particles
journal, August 2009

  • Nordlund, Gustav; Sing Ng, Jovice Boon; Bergström, Lennart
  • ACS Nano, Vol. 3, Issue 9
  • DOI: 10.1021/nn9005413

Experimental Models of Primitive Cellular Compartments: Encapsulation, Growth, and Division
journal, October 2003


Microcapsules Containing a Biomolecular Motor for ATP Biosynthesis
journal, August 2008


Synthetic cellularity based on non-lipid micro-compartments and protocell models
journal, October 2014


Plasmonic Colloidosomes as Three-Dimensional SERS Platforms with Enhanced Surface Area for Multiphase Sub-Microliter Toxin Sensing
journal, June 2015

  • Phan-Quang, Gia Chuong; Lee, Hiang Kwee; Phang, In Yee
  • Angewandte Chemie, Vol. 127, Issue 33
  • DOI: 10.1002/ange.201504027

Spontaneous Growth and Division in Self-Reproducing Inorganic Colloidosomes
journal, May 2014


Oriented adsorption of purple membrane to cationic surfaces
journal, May 1978


Colloidosomes: Selectively Permeable Capsules Composed of Colloidal Particles
journal, November 2002

  • Dinsmore, A. D.; Hsu, M. F.; Nikolaides, M. G.
  • Science, Vol. 298, Issue 5595, p. 1006-1009
  • DOI: 10.1126/science.1074868

Oriented Bacteriorhodopsin/Polycation Multilayers by Electrostatic Layer-by-Layer Assembly
journal, March 1998

  • He, Jin-An; Samuelson, Lynne; Li, Lian
  • Langmuir, Vol. 14, Issue 7
  • DOI: 10.1021/la971336y

Engineering Compartmentalized Biomimetic Micro- and Nanocontainers
journal, July 2017


Multifunctional Porous Microspheres Based on Peptide-Porphyrin Hierarchical Co-Assembly
journal, January 2014


The Origin of Membrane Bioenergetics
journal, December 2012


Microfluidic Formation of Monodisperse Coacervate Organelles in Liposomes
journal, July 2017

  • Deng, Nan-Nan; Huck, Wilhelm T. S.
  • Angewandte Chemie International Edition, Vol. 56, Issue 33
  • DOI: 10.1002/anie.201703145

Plasmonic Colloidosomes as Three-Dimensional SERS Platforms with Enhanced Surface Area for Multiphase Sub-Microliter Toxin Sensing
journal, June 2015

  • Phan-Quang, Gia Chuong; Lee, Hiang Kwee; Phang, In Yee
  • Angewandte Chemie International Edition, Vol. 54, Issue 33
  • DOI: 10.1002/anie.201504027

Controlled Assembly of Nanoparticle-Containing Gold and Silica Microspheres and Silica/Gold Nanocomposite Spheroids with Complex Form
journal, January 2003

  • Kulak, Alexander; Davis, Sean A.; Dujardin, Erik
  • Chemistry of Materials, Vol. 15, Issue 2
  • DOI: 10.1021/cm021259e

Metal Nanoparticle Plasmon-Enhanced Light-Harvesting in a Photosystem I Thin Film
journal, August 2011

  • Kim, Iltai; Bender, Shana L.; Hranisavljevic, Jasmina
  • Nano Letters, Vol. 11, Issue 8
  • DOI: 10.1021/nl2010109

In vitro gene expression and enzyme catalysis in bio-inorganic protocells
journal, January 2011

  • Li, Mei; Green, David C.; Anderson, J. L. Ross
  • Chemical Science, Vol. 2, Issue 9
  • DOI: 10.1039/c1sc00183c

Fourier transform infrared double-flash experiments resolve bacteriorhodopsin's M1 to M2 transition
journal, October 1997


Colloidal capsules: nano- and microcapsules with colloidal particle shells
journal, January 2017

  • Bollhorst, Tobias; Rezwan, Kurosch; Maas, Michael
  • Chemical Society Reviews, Vol. 46, Issue 8
  • DOI: 10.1039/C6CS00632A

High-Performance Bioassisted Nanophotocatalyst for Hydrogen Production
journal, June 2013

  • Balasubramanian, Shankar; Wang, Peng; Schaller, Richard D.
  • Nano Letters, Vol. 13, Issue 7
  • DOI: 10.1021/nl4016655

Light Controlled Reversible Inversion of Nanophosphor-Stabilized Pickering Emulsions for Biphasic Enantioselective Biocatalysis
journal, May 2014

  • Chen, Zhaowei; Zhou, Li; Bing, Wei
  • Journal of the American Chemical Society, Vol. 136, Issue 20
  • DOI: 10.1021/ja503123m

Phagocytosis-inspired behaviour in synthetic protocell communities of compartmentalized colloidal objects
journal, June 2017

  • Rodríguez-Arco, Laura; Li, Mei; Mann, Stephen
  • Nature Materials, Vol. 16, Issue 8
  • DOI: 10.1038/nmat4916

Chemical Signaling and Functional Activation in Colloidosome-Based Protocells
journal, February 2016


pH-sensitive vibrational probe reveals a cytoplasmic protonated cluster in bacteriorhodopsin
journal, December 2017

  • Lorenz-Fonfria, Victor A.; Saita, Mattia; Lazarova, Tzvetana
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 51
  • DOI: 10.1073/pnas.1707993114

Microfluidic Formation of Monodisperse Coacervate Organelles in Liposomes
journal, July 2017


On the origin of genomes and cells within inorganic compartments
journal, December 2005


The Influence of a Transmembrane pH Gradient on Protonation Probabilities of Bacteriorhodopsin: The Structural Basis of the Back-Pressure Effect
journal, June 2004


Chemical mapping of a single molecule by plasmon-enhanced Raman scattering
journal, June 2013


Black Gold: Plasmonic Colloidosomes with Broadband Absorption Self-Assembled from Monodispersed Gold Nanospheres by Using a Reverse Emulsion System
journal, June 2015

  • Liu, Dilong; Zhou, Fei; Li, Cuncheng
  • Angewandte Chemie International Edition, Vol. 54, Issue 33
  • DOI: 10.1002/anie.201503384

Individual Surface-Engineered Microorganisms as Robust Pickering Interfacial Biocatalysts for Resistance-Minimized Phase-Transfer Bioconversion
journal, February 2015


The early evolution of lipid membranes and the three domains of life
journal, June 2012

  • Lombard, Jonathan; López-García, Purificación; Moreira, David
  • Nature Reviews Microbiology, Vol. 10, Issue 7
  • DOI: 10.1038/nrmicro2815

Colloidal Jamming at Interfaces: A Route to Fluid-Bicontinuous Gels
journal, September 2005

  • Stratford, K.; Adhikari, R.; Pagonabarraga, I.
  • Science, Vol. 309, Issue 5744, p. 2198-2201
  • DOI: 10.1126/science.1116589