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Bacterial biofilms are highly abundant 3D living materials capable of performing complex biomechanical and biochemical functions, including programmable growth, self‐repair, filtration, and bioproduction. Methods to measure internal mechanical properties of biofilms in vivo with spatial resolution on the cellular scale have been lacking. Here, thousands of cells are tracked inside living 3D biofilms of the bacteriumVibrio choleraeduring and after the application of shear stress, for a wide range of stress amplitudes, periods, and biofilm sizes, which revealed anisotropic elastic and plastic responses of both cell displacements and cell reorientations. Using cellular tracking to infer parameters of a general mechanical model, spatially‐resolved measurements of the elastic modulus inside the biofilm are obtained, which correlate with the spatial distribution of the polysaccharides within the biofilm matrix. The noninvasive microrheology and force‐inference approach introduced here provides a general framework for studying mechanical properties with high spatial resolution in living materials.

 

Hyperuniformity, the suppression of density fluctuations at large length scales, is observed across a wide variety of domains, from cosmology to condensed matter and biological systems. Although the standard definition of hyperuniformity only utilizes information at the largest scales, hyperuniform configurations have distinctive local characteristics. However, the influence of global hyperuniformity on local structure has remained largely unexplored; establishing this connection can help uncover long-range interaction mechanisms and detect hyperuniform traits in finite-size systems. Here, we study the topological properties of hyperuniform point clouds by characterizing their persistent homology and the statistics of local graph neighborhoods. We find that varying the structure factor results in configurations with systematically different topological properties. Moreover, these topological properties are conserved for subsets of hyperuniform point clouds, establishing a connection between finite-sized systems and idealized reference arrangements. Comparing distributions of local topological neighborhoods reveals that the hyperuniform arrangements lie along a primarily one-dimensional manifold reflecting an order-to-disorder transition via hyperuniform configurations. The results presented here complement existing characterizations of hyperuniform phases of matter, and they show how local topological features can be used to detect hyperuniformity in size-limited simulations and experiments.

Published by the American Physical Society2024 

Complex disordered matter is of central importance to a wide range of disciplines, from bacterial colonies and embryonic tissues in biology to foams and granular media in materials science to stellar configurations in astrophysics. Because of the vast differences in composition and scale, comparing structural features across such disparate systems remains challenging. Here, by using the statistical properties of Delaunay tessellations, we introduce a mathematical framework for measuring topological distances between general three-dimensional point clouds. The resulting system-agnostic metric reveals subtle structural differences between bacterial biofilms as well as between zebrafish brain regions, and it recovers temporal ordering of embryonic development. We apply the metric to construct a universal topological atlas encompassing bacterial biofilms, snowflake yeast, plant shoots, zebrafish brain matter, organoids, and embryonic tissues as well as foams, colloidal packings, glassy materials, and stellar configurations. Living systems localize within a bounded island-like region of the atlas, reflecting that biological growth mechanisms result in characteristic topological properties.

 

Development of microbial communities is a complex multiscale phenomenon with wide-ranging biomedical and ecological implications. How biological and physical processes determine emergent spatial structures in microbial communities remains poorly understood due to a lack of simultaneous measurements of gene expression and cellular behaviour in space and time. Here we combined live-cell microscopy with a robotic arm for spatiotemporal sampling, which enabled us to simultaneously acquire phenotypic imaging data and spatiotemporal transcriptomes duringBacillus subtilisswarm development. Quantitative characterization of the spatiotemporal gene expression patterns revealed correlations with cellular and collective properties, and phenotypic subpopulations. By integrating these data with spatiotemporal metabolome measurements, we discovered a spatiotemporal cross-feeding mechanism fuelling swarm development: during their migration, earlier generations deposit metabolites which are consumed by later generations that swarm across the same location. These results highlight the importance of spatiotemporal effects during the emergence of phenotypic subpopulations and their interactions in bacterial communities.

 

Bacterial biofilms are among the most abundant multicellular structures on Earth and play essential roles in a wide range of ecological, medical, and industrial processes. However, general principles that govern the emergence of biofilm architecture across different species remain unknown. Here, we combine experiments, simulations, and statistical analysis to identify shared biophysical mechanisms that determine early biofilm architecture development at the single-cell level, for the species Vibrio cholerae , Escherichia coli , Salmonella enterica , and Pseudomonas aeruginosa grown as microcolonies in flow chambers. Our data-driven analysis reveals that despite the many molecular differences between these species, the biofilm architecture differences can be described by only 2 control parameters: cellular aspect ratio and cell density. Further experiments using single-species mutants for which the cell aspect ratio and the cell density are systematically varied, and mechanistic simulations show that tuning these 2 control parameters reproduces biofilm architectures of different species. Altogether, our results show that biofilm microcolony architecture is determined by mechanical cell–cell interactions, which are conserved across different species. 

Abstract Multicellular systems, from bacterial biofilms to human organs, form interfaces (or boundaries) between different cell collectives to spatially organize versatile functions 1,2 . The evolution of sufficiently descriptive genetic toolkits probably triggered the explosion of complex multicellular life and patterning 3,4 . Synthetic biology aims to engineer multicellular systems for practical applications and to serve as a build-to-understand methodology for natural systems 5–8 . However, our ability to engineer multicellular interface patterns 2,9 is still very limited, as synthetic cell–cell adhesion toolkits and suitable patterning algorithms are underdeveloped 5,7,10–13 . 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 materials 5–8,14 . 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 systems 3,5 .