Fluid flow drives phenotypic heterogeneity in bacterial growth and adhesion on surfaces

Antoine Hubert, Hervé Tabuteau (), Julien Farasin, Aleksandar Loncar, Alexis Dufresne, Yves Méheust and Tanguy Borgne ()
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Antoine Hubert: UMR 6118 University of Rennes and CNRS
Hervé Tabuteau: UMR 6251 University of Rennes and CNRS
Julien Farasin: UMR 6118 University of Rennes and CNRS
Aleksandar Loncar: UMR 6118 University of Rennes and CNRS
Alexis Dufresne: UMR 6553 University of Rennes and CNRS
Yves Méheust: UMR 6118 University of Rennes and CNRS
Tanguy Borgne: UMR 6118 University of Rennes and CNRS

Nature Communications, 2024, vol. 15, issue 1, 1-13

Abstract: Abstract Bacteria often thrive in surface-attached communities, where they can form biofilms affording them multiple advantages. In this sessile form, fluid flow is a key component of their environments, renewing nutrients and transporting metabolic products and signaling molecules. It also controls colonization patterns and growth rates on surfaces, through bacteria transport, attachment and detachment. However, the current understanding of bacterial growth on surfaces neglects the possibility that bacteria may modulate their division behavior as a response to flow. Here, we employed single-cell imaging in microfluidic experiments to demonstrate that attached Escherichia coli cells can enter a growth arrest state while simultaneously enhancing their adhesion underflow. Despite utilizing clonal populations, we observed a non-uniform response characterized by bistable dynamics, with co-existing subpopulations of non-dividing and actively dividing bacteria. As the proportion of non-dividing bacteria increased with the applied flow rate, it resulted in a reduction in the average growth rate of bacterial populations on flow-exposed surfaces. Dividing bacteria exhibited asymmetric attachment, whereas non-dividing counterparts adhered to the surface via both cell poles. Hence, this phenotypic diversity allows bacterial colonies to combine enhanced attachment with sustained growth, although at a reduced rate, which may be a significant advantage in fluctuating flow conditions.

Date: 2024
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DOI: 10.1038/s41467-024-49997-1

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