Microfluidic-based transcriptomics reveal force-independent bacterial rheosensing.

TitleMicrofluidic-based transcriptomics reveal force-independent bacterial rheosensing.
Publication TypeJournal Article
Year of Publication2019
AuthorsSanfilippo, JE, Lorestani, A, Koch, MD, Bratton, BP, Siryaporn, A, Stone, HA, Gitai, Z
JournalNat Microbiol
Volume4
Issue8
Pagination1274-1281
Date Published2019 08
ISSN2058-5276
KeywordsBacteria, Biofilms, Gene Expression Regulation, Bacterial, Genes, Bacterial, Microfluidics, Operon, Pseudomonas aeruginosa, Rheology, Sigma Factor, Transcriptome
Abstract

<p>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 force. 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.</p>

DOI10.1038/s41564-019-0455-0
Alternate JournalNat Microbiol
PubMed ID31086313
PubMed Central IDPMC6656604
Grant ListDP1 AI124669 / AI / NIAID NIH HHS / United States
K22 AI112816 / AI / NIAID NIH HHS / United States
R21 AI121828 / AI / NIAID NIH HHS / United States