Localized cell death focuses mechanical forces during 3D patterning in a biofilm
Edited by Herbert Levine, University of California at San Diego, La Jolla, CA, and approved August 27, 2012 (received for review July 19, 2012)
Commentary
November 1, 2012
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.
Acknowledgments
We thank Drs. M. Heinemann, M. Lehrman, S. Lockless, M. Rosen, R. Ranganathan, K. Süel, and D. Sprinzak and members of the G.M.S. laboratory for comments on the manuscript; Drs. W. Winkler, R. Kolter, and K. Pogliano for kindly providing bacterial strains; and H. Wu for analyzing time-lapse images. H.L. acknowledges funding from National Science Foundation Grants DMR-0907291, CMMI-1031829, and 1132174 and National Institutes of Health Grants 1 R01 EB013212 and 1 R01 DC011585. J.G.O. acknowledges funding from Grant FIS2009-13360 from the Spanish Ministry of Economy and Competitiveness and the Institució Catalana de Recerca i Estudis Avançats Academia Programme. This research was funded by National Institutes of Health National Institute of General Medical Sciences Grant R01 GM088428 and James S. McDonnell Foundation Grant 220020141 (both to G.M.S.).
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Freely available online through the PNAS open access option.
Submission history
Published online: September 24, 2012
Published in issue: November 13, 2012
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Acknowledgments
We thank Drs. M. Heinemann, M. Lehrman, S. Lockless, M. Rosen, R. Ranganathan, K. Süel, and D. Sprinzak and members of the G.M.S. laboratory for comments on the manuscript; Drs. W. Winkler, R. Kolter, and K. Pogliano for kindly providing bacterial strains; and H. Wu for analyzing time-lapse images. H.L. acknowledges funding from National Science Foundation Grants DMR-0907291, CMMI-1031829, and 1132174 and National Institutes of Health Grants 1 R01 EB013212 and 1 R01 DC011585. J.G.O. acknowledges funding from Grant FIS2009-13360 from the Spanish Ministry of Economy and Competitiveness and the Institució Catalana de Recerca i Estudis Avançats Academia Programme. This research was funded by National Institutes of Health National Institute of General Medical Sciences Grant R01 GM088428 and James S. McDonnell Foundation Grant 220020141 (both to G.M.S.).
Notes
*This Direct Submission article had a prearranged editor.
See Commentary on page 18633.
Authors
Competing Interests
The authors declare no conflict of interest.
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