Morphogenesis and cell ordering in confined bacterial biofilms
<jats:p>Biofilms are aggregates of bacterial cells surrounded by an extracellular matrix. Much progress has been made in studying biofilm growth on solid substrates; however, little is known about the biophysical mechanisms underlying biofilm development in three-dimensional confined environme...
| Hlavní autoři: | , , , , , , , |
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| Médium: | Článek |
| Jazyk: | English |
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Proceedings of the National Academy of Sciences
2021
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| On-line přístup: | https://hdl.handle.net/1721.1/132781 |
| _version_ | 1826212413600432128 |
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| author | Zhang, Qiuting Li, Jian Nijjer, Japinder Lu, Haoran Kothari, Mrityunjay Alert, Ricard Cohen, Tal Yan, Jing |
| author2 | Massachusetts Institute of Technology. Department of Civil and Environmental Engineering |
| author_facet | Massachusetts Institute of Technology. Department of Civil and Environmental Engineering Zhang, Qiuting Li, Jian Nijjer, Japinder Lu, Haoran Kothari, Mrityunjay Alert, Ricard Cohen, Tal Yan, Jing |
| author_sort | Zhang, Qiuting |
| collection | MIT |
| description | <jats:p>Biofilms are aggregates of bacterial cells surrounded by an extracellular matrix. Much progress has been made in studying biofilm growth on solid substrates; however, little is known about the biophysical mechanisms underlying biofilm development in three-dimensional confined environments in which the biofilm-dwelling cells must push against and even damage the surrounding environment to proliferate. Here, combining single-cell imaging, mutagenesis, and rheological measurement, we reveal the key morphogenesis steps of <jats:italic>Vibrio cholerae</jats:italic> biofilms embedded in hydrogels as they grow by four orders of magnitude from their initial size. We show that the morphodynamics and cell ordering in embedded biofilms are fundamentally different from those of biofilms on flat surfaces. Treating embedded biofilms as inclusions growing in an elastic medium, we quantitatively show that the stiffness contrast between the biofilm and its environment determines biofilm morphology and internal architecture, selecting between spherical biofilms with no cell ordering and oblate ellipsoidal biofilms with high cell ordering. When embedded in stiff gels, cells self-organize into a bipolar structure that resembles the molecular ordering in nematic liquid crystal droplets. In vitro biomechanical analysis shows that cell ordering arises from stress transmission across the biofilm–environment interface, mediated by specific matrix components. Our imaging technique and theoretical approach are generalizable to other biofilm-forming species and potentially to biofilms embedded in mucus or host tissues as during infection. Our results open an avenue to understand how confined cell communities grow by means of a compromise between their inherent developmental program and the mechanical constraints imposed by the environment.</jats:p> |
| first_indexed | 2024-09-23T15:20:58Z |
| format | Article |
| id | mit-1721.1/132781 |
| institution | Massachusetts Institute of Technology |
| language | English |
| last_indexed | 2024-09-23T15:20:58Z |
| publishDate | 2021 |
| publisher | Proceedings of the National Academy of Sciences |
| record_format | dspace |
| spelling | mit-1721.1/1327812024-05-31T21:02:27Z Morphogenesis and cell ordering in confined bacterial biofilms Zhang, Qiuting Li, Jian Nijjer, Japinder Lu, Haoran Kothari, Mrityunjay Alert, Ricard Cohen, Tal Yan, Jing Massachusetts Institute of Technology. Department of Civil and Environmental Engineering Massachusetts Institute of Technology. Department of Mechanical Engineering <jats:p>Biofilms are aggregates of bacterial cells surrounded by an extracellular matrix. Much progress has been made in studying biofilm growth on solid substrates; however, little is known about the biophysical mechanisms underlying biofilm development in three-dimensional confined environments in which the biofilm-dwelling cells must push against and even damage the surrounding environment to proliferate. Here, combining single-cell imaging, mutagenesis, and rheological measurement, we reveal the key morphogenesis steps of <jats:italic>Vibrio cholerae</jats:italic> biofilms embedded in hydrogels as they grow by four orders of magnitude from their initial size. We show that the morphodynamics and cell ordering in embedded biofilms are fundamentally different from those of biofilms on flat surfaces. Treating embedded biofilms as inclusions growing in an elastic medium, we quantitatively show that the stiffness contrast between the biofilm and its environment determines biofilm morphology and internal architecture, selecting between spherical biofilms with no cell ordering and oblate ellipsoidal biofilms with high cell ordering. When embedded in stiff gels, cells self-organize into a bipolar structure that resembles the molecular ordering in nematic liquid crystal droplets. In vitro biomechanical analysis shows that cell ordering arises from stress transmission across the biofilm–environment interface, mediated by specific matrix components. Our imaging technique and theoretical approach are generalizable to other biofilm-forming species and potentially to biofilms embedded in mucus or host tissues as during infection. Our results open an avenue to understand how confined cell communities grow by means of a compromise between their inherent developmental program and the mechanical constraints imposed by the environment.</jats:p> 2021-10-07T15:33:01Z 2021-10-07T15:33:01Z 2021-08 2021-04 2021-10-06T16:21:24Z Article http://purl.org/eprint/type/JournalArticle 1091-6490 https://hdl.handle.net/1721.1/132781 Qiuting Zhang, Jian Li, Japinder Nijjer, Haoran Lu, Mrityunjay Kothari, Ricard Alert, Tal Cohen, Jing Yan, Morphogenesis and cell ordering in confined bacterial biofilms, Proceedings of the National Academy of Sciences Aug 2021, 118 (31) en 10.1073/pnas.2107107118 Proceedings of the National Academy of Sciences Article is made available in accordance with the publisher's policy and may be subject to US copyright law. Please refer to the publisher's site for terms of use. application/pdf Proceedings of the National Academy of Sciences PNAS |
| spellingShingle | Zhang, Qiuting Li, Jian Nijjer, Japinder Lu, Haoran Kothari, Mrityunjay Alert, Ricard Cohen, Tal Yan, Jing Morphogenesis and cell ordering in confined bacterial biofilms |
| title | Morphogenesis and cell ordering in confined bacterial biofilms |
| title_full | Morphogenesis and cell ordering in confined bacterial biofilms |
| title_fullStr | Morphogenesis and cell ordering in confined bacterial biofilms |
| title_full_unstemmed | Morphogenesis and cell ordering in confined bacterial biofilms |
| title_short | Morphogenesis and cell ordering in confined bacterial biofilms |
| title_sort | morphogenesis and cell ordering in confined bacterial biofilms |
| url | https://hdl.handle.net/1721.1/132781 |
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