Surface-attached bacterial biofilms are self-replicating active liquid crystals and the dominant form of bacterial life on Earth1,2,3,4. In conventional liquid crystals and solid-state materials, the interaction potentials between the molecules that comprise the system determine the material properties. However, for growth-active biofilms it is unclear whether potential-based descriptions can account for the experimentally observed morphologies, and which potentials would be relevant. Here, we have overcome previous limitations of single-cell imaging techniques5,6 to reconstruct and track all individual cells inside growing three-dimensional biofilms with up to 10,000 individuals. Based on these data, we identify, constrain and provide a microscopic basis for an effective cell–cell interaction potential, which captures and predicts the growth dynamics, emergent architecture and local liquid-crystalline order of Vibrio cholerae biofilms. Furthermore, we show how external fluid flows control the microscopic structure and three-dimensional morphology of biofilms. Our analysis implies that local cellular order and global biofilm architecture in these active bacterial communities can arise from mechanical cell–cell interactions, which cells can modulate by regulating the production of particular matrix components. These results establish an experimentally validated foundation for improved continuum theories of active matter and thereby contribute to solving the important problem of controlling biofilm growth.
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The authors thank L. Vidakovic for contributions to bacterial strain creation, N. Netter and E. Jelli for preparing the graphics processing unit-based simulations to be run on the Max Planck Computing and Data Facility cluster, and C. Nadell and all members of the Drescher lab for discussions. This work was supported by grants from the Max Planck Society, the Human Frontier Science Program (CDA00084/2015-C), the European Research Council (StG-716734), the Deutsche Forschungsgemeinschaft (DFG) via the SFB987 framework to K.D., a MIT OGE Chyn Duog Shiah Memorial Fellowship to R.M., a James S. McDonnell Foundation Complex Systems Scholar Award and an Edmund F. Kelly Research Award to J.D., and an MIT-Germany MISTI Seed Grant to K.D. and J.D.
The authors declare no competing interests.
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Supplementary Information, Supplementary Data, Supplementary Figures 1–25, Supplementary Tables 1–7, Supplementary References 1–32
Biofilm formation of the WT* strain grown at low shear rate (γ = 2 s–1). Cells originating from the biofilm founder cell are labelled in blue
Biofilm formation of the ΔrbmA mutant grown at low shear rate (γ = 2 s–1). Cells originating from the biofilm founder cell are labelled in blue
Biofilm formation of the WT* strain grown at high shear rate (γ = 2,000 s–1). Cells originating from the biofilm founder cell are labelled in blue
Biofilm formation of the ΔrbmA mutant grown at high shear rate (γ = 660 s–1). Cells originating from the biofilm founder cell are labelled in blue
Simulated biofilm formation for the ΔrbmA mutant and the WT* strain using the best-fitting interaction potential for each case. Cells are colour-coded according to their local nematic order
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Hartmann, R., Singh, P.K., Pearce, P. et al. Emergence of three-dimensional order and structure in growing biofilms. Nat. Phys. 15, 251–256 (2019). https://doi.org/10.1038/s41567-018-0356-9
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