Localized cell death focuses mechanical forces during 3D patterning in a biofilm

Munehiro Asally, Mark Kittisopikul, Pau Rué, Yingjie Du, Zhenxing Hu, Tolga Çaǧatay, Andra B. Robinson, Hongbing Lu, Jordi Garcia-Ojalvo, Gürol M. Süel

Research output: Contribution to journalArticle

151 Citations (Scopus)

Abstract

From microbial biofilm communities to multicellular organisms, 3D macroscopic structures develop through poorly understood interplay between cellular processes and mechanical forces. Investigating wrinkled biofilms of Bacillus subtilis, we discovered a pattern of localized cell death that spatially focuses mechanical forces, and thereby initiates wrinkle formation. Deletion of genes implicated in biofilm development, together with mathematical modeling, revealed that ECM production underlies the localization of cell death. Simultaneously with cell death, we quantitatively measured mechanical stiffness and movement in WT and mutant biofilms. Results suggest that localized cell death provides an outlet for lateral compressive forces, thereby promoting vertical mechanical buckling, which subsequently leads to wrinkle formation. Guided by these findings, we were able to generate artificial wrinkle patterns within biofilms. Formation of 3D structures facilitated by cell death may underlie self-organization in other developmental systems, and could enable engineering of macroscopic structures from cell populations.

Original languageEnglish (US)
Pages (from-to)18891-18896
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume109
Issue number46
DOIs
StatePublished - Nov 13 2012

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Biofilms
Cell Death
Mechanical Phenomena
Gene Deletion
Bacillus subtilis
Population

Keywords

  • Pattern formation
  • Self-assembly
  • Systems dynamics

ASJC Scopus subject areas

  • General

Cite this

Localized cell death focuses mechanical forces during 3D patterning in a biofilm. / Asally, Munehiro; Kittisopikul, Mark; Rué, Pau; Du, Yingjie; Hu, Zhenxing; Çaǧatay, Tolga; Robinson, Andra B.; Lu, Hongbing; Garcia-Ojalvo, Jordi; Süel, Gürol M.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 109, No. 46, 13.11.2012, p. 18891-18896.

Research output: Contribution to journalArticle

Asally, M, Kittisopikul, M, Rué, P, Du, Y, Hu, Z, Çaǧatay, T, Robinson, AB, Lu, H, Garcia-Ojalvo, J & Süel, GM 2012, 'Localized cell death focuses mechanical forces during 3D patterning in a biofilm', Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 46, pp. 18891-18896. https://doi.org/10.1073/pnas.1212429109
Asally, Munehiro ; Kittisopikul, Mark ; Rué, Pau ; Du, Yingjie ; Hu, Zhenxing ; Çaǧatay, Tolga ; Robinson, Andra B. ; Lu, Hongbing ; Garcia-Ojalvo, Jordi ; Süel, Gürol M. / Localized cell death focuses mechanical forces during 3D patterning in a biofilm. In: Proceedings of the National Academy of Sciences of the United States of America. 2012 ; Vol. 109, No. 46. pp. 18891-18896.
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AU - Asally, Munehiro

AU - Kittisopikul, Mark

AU - Rué, Pau

AU - Du, Yingjie

AU - Hu, Zhenxing

AU - Çaǧatay, Tolga

AU - Robinson, Andra B.

AU - Lu, Hongbing

AU - Garcia-Ojalvo, Jordi

AU - Süel, Gürol M.

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AB - From microbial biofilm communities to multicellular organisms, 3D macroscopic structures develop through poorly understood interplay between cellular processes and mechanical forces. Investigating wrinkled biofilms of Bacillus subtilis, we discovered a pattern of localized cell death that spatially focuses mechanical forces, and thereby initiates wrinkle formation. Deletion of genes implicated in biofilm development, together with mathematical modeling, revealed that ECM production underlies the localization of cell death. Simultaneously with cell death, we quantitatively measured mechanical stiffness and movement in WT and mutant biofilms. Results suggest that localized cell death provides an outlet for lateral compressive forces, thereby promoting vertical mechanical buckling, which subsequently leads to wrinkle formation. Guided by these findings, we were able to generate artificial wrinkle patterns within biofilms. Formation of 3D structures facilitated by cell death may underlie self-organization in other developmental systems, and could enable engineering of macroscopic structures from cell populations.

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