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Nat Microbiol. 2019 Aug;4(8):1274-1281. doi: 10.1038/s41564-019-0455-0. Epub 2019 May 13.

Microfluidic-based transcriptomics reveal force-independent bacterial rheosensing.

Author information

1
Department of Molecular Biology, Princeton University, Princeton, NJ, USA.
2
Lewis-Sigler Institute for Integrative Genomics, Princeton University, Princeton, NJ, USA.
3
Department of Physics and Astronomy, University of California, Irvine, Irvine, CA, USA.
4
Department of Molecular Biology and Biochemistry, University of California, Irvine, Irvine, CA, USA.
5
Department of Mechanical and Aerospace Engineering, Princeton University, Princeton, NJ, USA.
6
Department of Molecular Biology, Princeton University, Princeton, NJ, USA. zgitai@princeton.edu.

Abstract

Multiple cell types sense fluid flow as an environmental cue. Flow can exert shear force (or stress) on cells, and the prevailing model is that biological flow sensing involves the measurement of shear force1,2. Here, we provide evidence for force-independent flow sensing in the bacterium Pseudomonas aeruginosa. A microfluidic-based transcriptomic approach enabled us to discover an operon of P. aeruginosa that is rapidly and robustly upregulated in response to flow. Using a single-cell reporter of this operon, which we name the flow-regulated operon (fro), we establish that P. aeruginosa dynamically tunes gene expression to flow intensity through a process we call rheosensing (as rheo- is Greek for flow). We further show that rheosensing occurs in multicellular biofilms, involves signalling through the alternative sigma factor FroR, and does not require known surface sensors. To directly test whether rheosensing measures force, we independently altered the two parameters that contribute to shear stress: shear rate and solution viscosity. Surprisingly, we discovered that rheosensing is sensitive to shear rate but not viscosity, indicating that rheosensing is a kinematic (force-independent) form of mechanosensing. Thus, our findings challenge the dominant belief that biological mechanosensing requires the measurement of forces.

PMID:
31086313
PMCID:
PMC6656604
[Available on 2019-11-13]
DOI:
10.1038/s41564-019-0455-0

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