Abstract
The design and assembly of artificial protocell consortia displaying dynamical behaviours and systems-based properties are emerging challenges in bottom-up synthetic biology. Cellular processes such as morphogenesis and differentiation rely in part on reaction-diffusion gradients, and the ability to mimic rudimentary aspects of these non-equilibrium processes in communities of artificial cells could provide a step to life-like systems capable of complex spatiotemporal transformations. Here we expose acoustically formed arrays of initially identical coacervate micro-droplets to uni-directional or counter-directional reaction-diffusion gradients of artificial morphogens to induce morphological differentiation and spatial patterning in single populations of model protocells. Dynamic reconfiguration of the droplets in the morphogen gradients produces a diversity of membrane-bounded vesicles that are spontaneously segregated into multimodal populations with differentiated enzyme activities. Our results highlight the opportunities for constructing protocell arrays with graded structure and functionality and provide a step towards the development of artificial cell platforms capable of multiple operations.
Highlights
The design and assembly of artificial protocell consortia displaying dynamical behaviours and systems-based properties are emerging challenges in bottom-up synthetic biology
By using intersecting chemical gradients generated under different morphogen molar ratios we demonstrate that a range of organized protocell consortia can be produced under non-equilibrium conditions
We show that encapsulation of horseradish peroxidase within the coacervate droplets leads to differentiated protocell communities that exhibit spatially dependent enzymatic responses when exposed to identical substrate concentrations principally due to morphogen-induced changes in vesicle membrane permeability
Summary
The above results indicated that the transformation of acoustically formed PDDA/ATP coacervate micro-droplets in the presence of a homogeneous solution of polyanionic POM clusters produced three distinct types of membrane-bounded coacervate vesicles as the concentration of the additive was increased from 0.5 to 2 mM (Supplementary Fig. 10). Given that POM clusters and SDS micelles were both capable of concentration-dependent restructuring of the PDDA/ATP coacervate micro-droplets under equilibrium conditions, we sought to exploit these additives as artificial morphogens for generating spatiotemporal patterns of chemical/physical differentiation in homogenous populations of initially identical model protocells. We prepared an acoustically formed square array of immobilized PDDA/ATP micro-droplets, switched off the acoustic pressure field and injected an aqueous solution of sodium phosphotungstate or SDS into the device from one edge of the chamber (Supplementary Fig. 1) to produce a unidirectional chemical gradient across the observation window of the device (Fig. 2a). Injection of an aqueous solution of the POM clusters to give a final concentration across the entire chamber after equilibration of 0.625 mM resulted in the spontaneous differentiation of the homogeneous population of coacervate droplets into a binary population of spherical (26%) and balloon-shaped (74%) membrane-bounded POM/coacervate vesicles
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