Orthogonal Light‐Dependent Membrane Adhesion Induces Social Self‐Sorting and Member‐Specific DNA Communication in Synthetic Cell Communities

Abstract

Intercellular communication is essential to coordinate the collective operation of individual cells and to establish multicellular structures with specialized cells. [ , ] For this, sender cells secrete signals in the form of diffusible chemicals which can be recognized by receiver cells within the signaling range and with appropriate receptors. Building similar capabilities into synthetic cells allows community-based functions and interactions among synthetic cells [ , ] and living cells. [ ] Remarkable achievements of communication in synthetic cells include communities that process DNA-coded information through reaction networks, [ ] mimic quorum sensing, [ , ] differentiate into different patterns, [ ] exhibit prey-predatory relationships, [ ] synchronization, [ ] and oscillations, [ , ] and regulate cellular behavior in response to physiological conditions. [ ] These studies illustrated how communication in synthetic cells helps to understand underlying organizational Developing orthogonal chemical communication pathways in diverse synthetic cell communities is a considerable challenge due to the increased crosstalk and interference associated with large numbers of different types of sender-receiver pairs. Herein, the authors control which sender-receiver pairs communicate in a three-membered community of synthetic cells through red and blue light illumination. Semipermeable protein-polymer-based synthetic cells (proteinosomes) with complementary membrane-attached protein adhesion communicate through single-stranded DNA oligomers and synergistically process biochemical information within a community consisting of one sender and two different receiver populations. Different pairs of red and blue light-responsive protein-protein interactions act as membrane adhesion mediators between the sender and receivers such that they self-assemble and socially self-sort into different multicellular structures under red and blue light. Consequently, distinct sender-receiver pairs come into the signaling range depending on the light illumination and are able to communicate specifically without activation of the other receiver population. Overall, this work shows how photoswitchable membrane adhesion gives rise to different self-sorting protocell patterns that mediate member-specific DNA-based communication in ternary populations of synthetic cells and provides a step towards the design of orthogonal chemical communication networks in diverse communities of synthetic cells.

Protocell Communication through the Eyes of Synthetic Organic Chemists

“…[15] Light was also used to cause selective aggregation of different proteinosome populations allowing the DSD reaction to occur. [16] Di Michele and coworkers improved on simple DSD-based communication by assembling DNA-based protocells responsive to diffusible chemical signals. These protocells were capable of responding to the addition of DNA strands by forming distinct internal architectures, and establishing complex communication networks with living cells.…”

“…moved this technology further, and successfully used light to trigger the DSD cascades [15] . Light was also used to cause selective aggregation of different proteinosome populations allowing the DSD reaction to occur [16] . Di Michele and co‐workers improved on simple DSD‐based communication by assembling DNA‐based protocells responsive to diffusible chemical signals.…”

Autonomic Integration in Nested Protocell Communities

“…Synthetic protobiology is concerned with the construction, reconstitution, and functionalization of individual cell-like entities, − development of living cell/synthetic cell constructs (cellular bionics) and signaling networks, − and implementation of protocell dynamics and chemical communication in populations of artificial cells. − Studies of dispersed protocell communities explore contact-dependent and through-space chemical interactions as steps toward the development of higher-order cytomimetic behaviors such as division and growth, prototissue assembly, − signal processing, ,− self-sorting, and DNA-based computation. , Nested communities of synthetic cells can be prepared by sequential processing or microfluidic techniques to produce vesicle-in-vesicle, proteinosome-in-proteinosome, polymersome-in-polymersome, polymersome-in-polymer capsule, coacervate-in-coacervate droplet, and living cell-in-vesicle , arrangements. Alternatively, properties such as wetting and interfacial tension can be utilized for the development of physically interactive artificial cell communities that exhibit behaviors such as artificial phagocytosis, parasitism, and predation − to produce nested protocells via mechanisms of engulfment, processing, and functional integration (artificial endosymbiosis).…”

Editorial for the Special Issue ‘Synthetic Biology and Biomimicry'

“…[18] De Greef, Kostiainen et al investigate protocells as scavengers for heparin. [19] Wegner et al [20] report on light-dependent adhesion phenomena in artificial membranes and synthetic cells.As guest editors of this special issue and co-organizers of the ArtBio2022 conference, we sincerely hope that both the physi cal event and this collection of articles contribute to the development and promotion of the exciting, fundamentally important field of bottom-up synthetic biology.…”

“…[18] De Greef, Kostiainen et al investigate protocells as scavengers for heparin. [19] Wegner et al [20] report on light-dependent adhesion phenomena in artificial membranes and synthetic cells.…”