TY - JOUR
T1 - Localized cell death focuses mechanical forces during 3D patterning in a biofilm
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.
PY - 2012/11/13
Y1 - 2012/11/13
N2 - 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.
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.
KW - Pattern formation
KW - Self-assembly
KW - Systems dynamics
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U2 - 10.1073/pnas.1212429109
DO - 10.1073/pnas.1212429109
M3 - Article
C2 - 23012477
AN - SCOPUS:84869234725
SN - 0027-8424
VL - 109
SP - 18891
EP - 18896
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
IS - 46
ER -