4-bit adhesion logic enables universal multicellular interface patterning

Honesty Kim, Dominic J. Skinner, David S. Glass, Alexander E. Hamby, Bradey A. R. Stuart, Jörn Dunkel and Ingmar H. Riedel-Kruse ()
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Honesty Kim: University of Arizona
Dominic J. Skinner: Massachusetts Institute of Technology
David S. Glass: Weizmann Institute of Science
Alexander E. Hamby: University of Arizona
Bradey A. R. Stuart: University of Arizona
Jörn Dunkel: Massachusetts Institute of Technology
Ingmar H. Riedel-Kruse: University of Arizona

Nature, 2022, vol. 608, issue 7922, 324-329

Abstract: Abstract Multicellular systems, from bacterial biofilms to human organs, form interfaces (or boundaries) between different cell collectives to spatially organize versatile functions1,2. The evolution of sufficiently descriptive genetic toolkits probably triggered the explosion of complex multicellular life and patterning3,4. Synthetic biology aims to engineer multicellular systems for practical applications and to serve as a build-to-understand methodology for natural systems5–8. However, our ability to engineer multicellular interface patterns2,9 is still very limited, as synthetic cell–cell adhesion toolkits and suitable patterning algorithms are underdeveloped5,7,10–13. Here we introduce a synthetic cell–cell adhesin logic with swarming bacteria and establish the precise engineering, predictive modelling and algorithmic programming of multicellular interface patterns. We demonstrate interface generation through a swarming adhesion mechanism, quantitative control over interface geometry and adhesion-mediated analogues of developmental organizers and morphogen fields. Using tiling and four-colour-mapping concepts, we identify algorithms for creating universal target patterns. This synthetic 4-bit adhesion logic advances practical applications such as human-readable molecular diagnostics, spatial fluid control on biological surfaces and programmable self-growing materials5–8,14. Notably, a minimal set of just four adhesins represents 4 bits of information that suffice to program universal tessellation patterns, implying a low critical threshold for the evolution and engineering of complex multicellular systems3,5.

Date: 2022
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DOI: 10.1038/s41586-022-04944-2

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