Cell. 2022 Jan 6;185(1):145-157.e13. doi: 10.1016/j.cell.2021.12.001. | PubMed

Kwang-Tao Chou¹, Dong-Yeon D Lee², Jian-Geng Chiou¹, Leticia Galera-Laporta¹, San Ly¹, Jordi Garcia-Ojalvo³, Gürol M Süel⁴

1. Molecular Biology Section, Division of Biological Sciences, University of California San Diego, La Jolla, CA 92093, USA.
2. Department of Bioengineering, Stanford University, Stanford, CA 94305, USA.
3. Department of Experimental and Health Sciences, Universitat Pompeu Fabra, 08003 Barcelona, Spain.
4. Molecular Biology Section, Division of Biological Sciences, University of California San Diego, La Jolla, CA 92093, USA; San Diego Center for Systems Biology, University of California San Diego, La Jolla, CA 92093-0380, USA; Center for Microbiome Innovation, University of California San Diego, La Jolla, CA 92093-0380, USA. Electronic address: gsuel@ucsd.edu.

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.

Presented By Todd Kwang-Tao Chou | ORCID iD