Bistable emergence of oscillations in growing Bacillus subtilis biofilms

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• dc.contributor.author Martínez Corral, Rosa, 1991-
• dc.contributor.author Liu, Jintao
• dc.contributor.author Süel, Gürol M.
• dc.contributor.author García Ojalvo, Jordi
• dc.date.accessioned 2019-07-12T07:52:47Z
• dc.date.available 2019-07-12T07:52:47Z
• dc.date.issued 2018
• dc.description.abstract Biofilm communities of Bacillus subtilis bacteria have recently been shown to exhibit collective growth-rate oscillations mediated by electrochemical signaling to cope with nutrient starvation. These oscillations emerge once the colony reaches a large enough number of cells. However, it remains unclear whether the amplitude of the oscillations, and thus their effectiveness, builds up over time gradually or if they can emerge instantly with a nonzero amplitude. Here we address this question by combining microfluidics-based time-lapse microscopy experiments with a minimal theoretical description of the system in the form of a delay-differential equation model. Analytical and numerical methods reveal that oscillations arise through a subcritical Hopf bifurcation, which enables instant high-amplitude oscillations. Consequently, the model predicts a bistable regime where an oscillating and a nonoscillating attractor coexist in phase space. We experimentally validate this prediction by showing that oscillations can be triggered by perturbing the media conditions, provided the biofilm size lies within an appropriate range. The model also predicts that the minimum size at which oscillations start decreases with stress, a fact that we also verify experimentally. Taken together, our results show that collective oscillations in cell populations can emerge suddenly with nonzero amplitude via a discontinuous transition.
• dc.description.sponsorship This work was supported by the Spanish Ministry of Economy and Competitiveness and Fondo Europeo de Desarrollo Regional (Project FIS2015-66503-C3-1-P) and by the Generalitat de Catalunya (Project 2017 SGR 1054). R.M.-C. acknowledges financial support from La Caixa Foundation. J.G.-O. acknowledges support from the Institució Catalana de Recerca i Estudis Avançats Academia programme and from the “María de Maeztu” Programme for Units of Excellence in Research and Development (Spanish Ministry of Economy and Competitiveness, MDM-2014-0370). J.L. acknowledges support from the J.L. acknowledges support from the Tsinghua–Peking Center for Life Sciences and the Thousand Talents Program of China. G.M.S. acknowledges support for this research from the San Diego Center for Systems Biology (NIH Grant P50 GM085764), the National Institute of General Medical Sciences (Grant R01 GM121888 to G.M.S.), the Defense Advanced Research Projects Agency (Grant HR0011-16-2-0035 to G.M.S.), and the Howard Hughes Medical Institute–Simons Foundation Faculty Scholars program (G.M.S.).
• dc.format.mimetype application/pdf
• dc.identifier.citation Martinez-Corral R, Liu J, Süel GM, Garcia-Ojalvo J. Bistable emergence of oscillations in growing Bacillus subtilis biofilms. Proc Natl Acad Sci U S A. 2018;115(36):8333-40. DOI: 10.1073/pnas.1805004115
• dc.identifier.doi http://dx.doi.org/10.1073/pnas.1805004115
• dc.identifier.issn 0027-8424
• dc.identifier.uri http://hdl.handle.net/10230/41990
• dc.language.iso eng
• dc.publisher National Academy of Sciences
• dc.relation.ispartof Proceedings of the National Academy of Sciences of the United States of America. 2018;115(36):8333-40
• dc.relation.projectID info:eu-repo/grantAgreement/ES/1PE/FIS2015-66503-C3-1-P
• dc.rights © National Academy of Sciences
• dc.rights.accessRights info:eu-repo/semantics/openAccess
• dc.subject.keyword Biofilm growth
• dc.subject.keyword Biological oscillations
• dc.subject.keyword Delay-induced oscillations
• dc.subject.keyword Delayed negative feedback
• dc.subject.keyword Subcritical Hopf bifurcation
• dc.title Bistable emergence of oscillations in growing Bacillus subtilis biofilms
• dc.type info:eu-repo/semantics/article
• dc.type.version info:eu-repo/semantics/acceptedVersion