Biofilms as self-shaping growing nematics
Active nematics are the non-equilibrium analogue of passive liquid crystals. They consist of anisotropic units that consume free energy to drive emergent behaviour. As with liquid crystal molecules in displays, ordering and dynamics in active nematics are sensitive to boundary conditions. However, u...
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Published in | Nature physics Vol. 19; no. 12; pp. 1936 - 1944 |
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Main Authors | , , , , , , , , , |
Format | Journal Article |
Language | English |
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01.12.2023
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Abstract | Active nematics are the non-equilibrium analogue of passive liquid crystals. They consist of anisotropic units that consume free energy to drive emergent behaviour. As with liquid crystal molecules in displays, ordering and dynamics in active nematics are sensitive to boundary conditions. However, unlike passive liquid crystals, active nematics have the potential to regulate their boundaries through self-generated stresses. Here we show how a three-dimensional, living nematic can actively shape itself and its boundary to regulate its internal architecture through growth-induced stresses, using bacterial biofilms confined by a hydrogel as a model system. We show that biofilms exhibit a sharp transition in shape from domes to lenses in response to changing environmental stiffness or cell–substrate friction, which is explained by a theoretical model that considers the competition between confinement and interfacial forces. The growth mode defines the progression of the boundary, which in turn determines the trajectories and spatial distribution of cell lineages. We further demonstrate that the evolving boundary and corresponding stress anisotropy define the orientational ordering of cells and the emergence of topological defects in the biofilm interior. Our findings may provide strategies for the development of programmed microbial consortia with emergent material properties.Confined biofilms can shape themselves and their boundary to modify their internal organisation. This mechanism could inform the development of active materials that control their own geometry. |
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AbstractList | Active nematics are the non-equilibrium analogue of passive liquid crystals. They consist of anisotropic units that consume free energy to drive emergent behaviour. As with liquid crystal molecules in displays, ordering and dynamics in active nematics are sensitive to boundary conditions. However, unlike passive liquid crystals, active nematics have the potential to regulate their boundaries through self-generated stresses. Here we show how a three-dimensional, living nematic can actively shape itself and its boundary to regulate its internal architecture through growth-induced stresses, using bacterial biofilms confined by a hydrogel as a model system. We show that biofilms exhibit a sharp transition in shape from domes to lenses in response to changing environmental stiffness or cell–substrate friction, which is explained by a theoretical model that considers the competition between confinement and interfacial forces. The growth mode defines the progression of the boundary, which in turn determines the trajectories and spatial distribution of cell lineages. We further demonstrate that the evolving boundary and corresponding stress anisotropy define the orientational ordering of cells and the emergence of topological defects in the biofilm interior. Our findings may provide strategies for the development of programmed microbial consortia with emergent material properties.Confined biofilms can shape themselves and their boundary to modify their internal organisation. This mechanism could inform the development of active materials that control their own geometry. Active nematics are the nonequilibrium analogue of passive liquid crystals. They consist of anisotropic units that consume free energy to drive emergent behaviour. Like liquid crystal molecules in displays, ordering and dynamics in active nematics are sensitive to boundary conditions. However, unlike passive liquid crystals, active nematics have the potential to regulate their boundaries through self-generated stresses. Here, we show how a three-dimensional, living nematic can actively shape itself and its boundary to regulate its internal architecture through growth-induced stresses, using bacterial biofilms confined by a hydrogel as a model system. We show that biofilms exhibit a sharp transition in shape from domes to lenses upon changing environmental stiffness or cell-substrate friction, which is explained by a theoretical model that considers the competition between confinement and interfacial forces. The growth mode defines the progression of the boundary, which in turn determines the trajectories and spatial distribution of cell lineages. We further demonstrate that the evolving boundary and corresponding stress anisotropy define the orientational ordering of cells and the emergence of topological defects in the biofilm interior. Our findings may provide strategies for the development of programmed microbial consortia with emergent material properties. Active nematics are the nonequilibrium analogue of passive liquid crystals. They consist of anisotropic units that consume free energy to drive emergent behaviour. Like liquid crystal molecules in displays, ordering and dynamics in active nematics are sensitive to boundary conditions. However, unlike passive liquid crystals, active nematics have the potential to regulate their boundaries through self-generated stresses. Here, we show how a three-dimensional, living nematic can actively shape itself and its boundary to regulate its internal architecture through growth-induced stresses, using bacterial biofilms confined by a hydrogel as a model system. We show that biofilms exhibit a sharp transition in shape from domes to lenses upon changing environmental stiffness or cell-substrate friction, which is explained by a theoretical model that considers the competition between confinement and interfacial forces. The growth mode defines the progression of the boundary, which in turn determines the trajectories and spatial distribution of cell lineages. We further demonstrate that the evolving boundary and corresponding stress anisotropy define the orientational ordering of cells and the emergence of topological defects in the biofilm interior. Our findings may provide strategies for the development of programmed microbial consortia with emergent material properties.Active nematics are the nonequilibrium analogue of passive liquid crystals. They consist of anisotropic units that consume free energy to drive emergent behaviour. Like liquid crystal molecules in displays, ordering and dynamics in active nematics are sensitive to boundary conditions. However, unlike passive liquid crystals, active nematics have the potential to regulate their boundaries through self-generated stresses. Here, we show how a three-dimensional, living nematic can actively shape itself and its boundary to regulate its internal architecture through growth-induced stresses, using bacterial biofilms confined by a hydrogel as a model system. We show that biofilms exhibit a sharp transition in shape from domes to lenses upon changing environmental stiffness or cell-substrate friction, which is explained by a theoretical model that considers the competition between confinement and interfacial forces. The growth mode defines the progression of the boundary, which in turn determines the trajectories and spatial distribution of cell lineages. We further demonstrate that the evolving boundary and corresponding stress anisotropy define the orientational ordering of cells and the emergence of topological defects in the biofilm interior. Our findings may provide strategies for the development of programmed microbial consortia with emergent material properties. |
Author | Nijjer, Japinder Li, Changhao Zhang, Qiuting Kothari, Mrityunjay Cohen, Tal Henzel, Thomas Yan, Jing Zhang, Sulin Tai, Jung-Shen B Zhou, Shuang |
AuthorAffiliation | 1 Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, CT, USA 8 Quantitative Biology Institute, Yale University, New Haven, CT, USA 4 Department of Mechanical Engineering, University of New Hampshire, Durham, NH, USA 3 Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA 6 Department of Mechanical Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA 5 Department of Physics, University of Massachusetts Amherst, Amherst, MA, USA 7 Department of Biomedical Engineering, Pennsylvania State University, University Park, PA, USA 2 Department of Engineering Science and Mechanics, Pennsylvania State University, University Park, PA, USA |
AuthorAffiliation_xml | – name: 1 Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, CT, USA – name: 5 Department of Physics, University of Massachusetts Amherst, Amherst, MA, USA – name: 3 Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA – name: 6 Department of Mechanical Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA – name: 4 Department of Mechanical Engineering, University of New Hampshire, Durham, NH, USA – name: 7 Department of Biomedical Engineering, Pennsylvania State University, University Park, PA, USA – name: 8 Quantitative Biology Institute, Yale University, New Haven, CT, USA – name: 2 Department of Engineering Science and Mechanics, Pennsylvania State University, University Park, PA, USA |
Author_xml | – sequence: 1 givenname: Japinder surname: Nijjer fullname: Nijjer, Japinder – sequence: 2 givenname: Changhao surname: Li fullname: Li, Changhao – sequence: 3 givenname: Mrityunjay surname: Kothari fullname: Kothari, Mrityunjay – sequence: 4 givenname: Thomas surname: Henzel fullname: Henzel, Thomas – sequence: 5 givenname: Qiuting surname: Zhang fullname: Zhang, Qiuting – sequence: 6 givenname: Jung-Shen B surname: Tai fullname: Tai, Jung-Shen B – sequence: 7 givenname: Shuang surname: Zhou fullname: Zhou, Shuang – sequence: 8 givenname: Tal surname: Cohen fullname: Cohen, Tal – sequence: 9 givenname: Sulin surname: Zhang fullname: Zhang, Sulin – sequence: 10 givenname: Jing surname: Yan fullname: Yan, Jing |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Author contributions: J.N. and C.L. contributed equally to the work. J.N. and J.Y. conceptualized the project. J.N. and Q.Z. performed the experiments and J.N. and J.-S.B.T. performed the data analysis. J.N., M.K., T.H., S.Z., T.C. and J.Y. formulated the theoretical model. C.L. and S.Z. developed the agent-based simulations. All authors contributed to the writing of the manuscript. |
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Snippet | Active nematics are the non-equilibrium analogue of passive liquid crystals. They consist of anisotropic units that consume free energy to drive emergent... Active nematics are the nonequilibrium analogue of passive liquid crystals. They consist of anisotropic units that consume free energy to drive emergent... |
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SubjectTerms | Active control Anisotropy Biofilms Boundary conditions Crystal defects Crystals Development strategies Environmental changes Free energy Liquid crystals Material properties Microorganisms Spatial distribution Stresses Substrates |
Title | Biofilms as self-shaping growing nematics |
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