A deterministic, c-di-GMP-dependent program ensures the generation of phenotypically similar, symmetric daughter cells during cytokinesis

María Pérez-Burgos, Marco Herfurth, Andreas Kaczmarczyk, Andrea Harms, Katrin Huber, Urs Jenal, Timo Glatter and Lotte Søgaard-Andersen ()
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María Pérez-Burgos: Max Planck Institute for Terrestrial Microbiology
Marco Herfurth: Max Planck Institute for Terrestrial Microbiology
Andreas Kaczmarczyk: University of Basel
Andrea Harms: Max Planck Institute for Terrestrial Microbiology
Katrin Huber: Max Planck Institute for Terrestrial Microbiology
Urs Jenal: University of Basel
Timo Glatter: Max Planck Institute for Terrestrial Microbiology
Lotte Søgaard-Andersen: Max Planck Institute for Terrestrial Microbiology

Nature Communications, 2024, vol. 15, issue 1, 1-20

Abstract: Abstract Phenotypic heterogeneity in bacteria can result from stochastic processes or deterministic programs. The deterministic programs often involve the versatile second messenger c-di-GMP, and give rise to daughter cells with different c-di-GMP levels by deploying c-di-GMP metabolizing enzymes asymmetrically during cell division. By contrast, less is known about how phenotypic heterogeneity is kept to a minimum. Here, we identify a deterministic c-di-GMP-dependent program that is hardwired into the cell cycle of Myxococcus xanthus to minimize phenotypic heterogeneity and guarantee the formation of phenotypically similar daughter cells during division. Cells lacking the diguanylate cyclase DmxA have an aberrant motility behaviour. DmxA is recruited to the cell division site and its activity is switched on during cytokinesis, resulting in a transient increase in the c-di-GMP concentration. During cytokinesis, this c-di-GMP burst ensures the symmetric incorporation and allocation of structural motility proteins and motility regulators at the new cell poles of the two daughters, thereby generating phenotypically similar daughters with correct motility behaviours. Thus, our findings suggest a general c-di-GMP-dependent mechanism for minimizing phenotypic heterogeneity, and demonstrate that bacteria can ensure the formation of dissimilar or similar daughter cells by deploying c-di-GMP metabolizing enzymes to distinct subcellular locations.

Date: 2024
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DOI: 10.1038/s41467-024-50444-4

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