A segmentation clock patterns cellular differentiation in a bacterial biofilm

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• dc.contributor.author Chou, Kwang-Tao
• dc.contributor.author Lee, Dong-yeon D.
• dc.contributor.author Chiou, Jian-Geng
• dc.contributor.author Galera Laporta, Letícia, 1985-
• dc.contributor.author Ly, San
• dc.contributor.author García Ojalvo, Jordi
• dc.contributor.author Süel, Gürol M.
• dc.date.accessioned 2023-04-21T06:15:22Z
• dc.date.available 2023-04-21T06:15:22Z
• dc.date.issued 2022
• dc.description.abstract Contrary to multicellular organisms that display segmentation during development, communities of unicellular organisms are believed to be devoid of such sophisticated patterning. Unexpectedly, we find that the gene expression underlying the nitrogen stress response of a developing Bacillus subtilis biofilm becomes organized into a ring-like pattern. Mathematical modeling and genetic probing of the underlying circuit indicate that this patterning is generated by a clock and wavefront mechanism, similar to that driving vertebrate somitogenesis. We experimentally validated this hypothesis by showing that predicted nutrient conditions can even lead to multiple concentric rings, resembling segments. We additionally confirmed that this patterning mechanism is driven by cell-autonomous oscillations. Importantly, we show that the clock and wavefront process also spatially patterns sporulation within the biofilm. Together, these findings reveal a biofilm segmentation clock that organizes cellular differentiation in space and time, thereby challenging the paradigm that such patterning mechanisms are exclusive to plant and animal development.
• dc.description.sponsorship We acknowledge Munehiro Asally, Tolga Çağatay, and Katherine Süel for helpful discussions. K.-T.C. acknowledges support from National Institutes of Health grant T32GM127235. J.G.-O. acknowledges support from the Spanish Ministry of Science, Innovation and Universities and FEDER (Project PGC2018-101251-B-I00 and CEX2018-000792-M), and from the Generalitat de Catalunya (ICREA Academia program). G.M.S. acknowledges support for this research from National Institute of General Medical Sciences grants R01 GM121888 and R35 GM139645. G.M.S. is a Howard Hughes Medical Institute - Simons Foundation Faculty Scholar.
• dc.format.mimetype application/pdf
• dc.identifier.citation Chou KT, Lee DD, Chiou JG, Galera-Laporta L, Ly S, Garcia-Ojalvo J, Süel GM. A segmentation clock patterns cellular differentiation in a bacterial biofilm. Cell. 2022;185(1):145-57.e13. DOI: 10.1016/j.cell.2021.12.001
• dc.identifier.doi http://dx.doi.org/10.1016/j.cell.2021.12.001
• dc.identifier.issn 0092-8674
• dc.identifier.uri http://hdl.handle.net/10230/56532
• dc.language.iso eng
• dc.publisher Elsevier
• dc.relation.ispartof Cell. 2022;185(1):145-57.e13
• dc.relation.projectID info:eu-repo/grantAgreement/ES/2PE/PGC2018-101251-B-I00
• dc.relation.projectID info:eu-repo/grantAgreement/ES/2PE/CEX2018-000792-M
• dc.rights © Elsevier http://dx.doi.org/10.1016/j.cell.2021.12.001
• dc.rights.accessRights info:eu-repo/semantics/openAccess
• dc.subject.keyword Bacillus subtilis
• dc.subject.keyword Biofilm
• dc.subject.keyword Clock and wavefront
• dc.subject.keyword Multicellularity
• dc.subject.keyword Nitrogen stress response
• dc.subject.keyword Pattern formation
• dc.subject.keyword Segmentation clock
• dc.subject.keyword Somitogenesis
• dc.subject.keyword Sporulation
• dc.title A segmentation clock patterns cellular differentiation in a bacterial biofilm
• dc.type info:eu-repo/semantics/article
• dc.type.version info:eu-repo/semantics/acceptedVersion