TY - JOUR
T1 - Microfluidic-based transcriptomics reveal force-independent bacterial rheosensing
AU - Sanfilippo, Joseph E.
AU - Lorestani, Alexander
AU - Koch, Matthias D.
AU - Bratton, Benjamin P.
AU - Siryaporn, Albert
AU - Stone, Howard A.
AU - Gitai, Zemer
N1 - Funding Information:
We thank K. Kim for assistance with generating the flow-shielded and biofilm streamer microfluidic channels. We also thank members of the Gitai laboratory, J. Shaevitz, N. Wingreen, D. Kearns and L. Wiltbank for helpful discussions and comments on the manuscript. This work was supported by a grant (DP1AI124669) from the National Institutes of Health (to Z.G.). Additional funding came from the National Science Foundation (PHY-1734030 to B.P.B. and M.D.K.), Glenn for Aging Research (B.P.B.), DFG award KO5239/1-1 from the German Research Foundation (to M.D.K.), and National Institutes of Health grants K22AI112816 (to A.S.) and R21AI121828 (to B.P.B. and M.D.K.).
Publisher Copyright:
© 2019, The Author(s), under exclusive licence to Springer Nature Limited.
PY - 2019/8/1
Y1 - 2019/8/1
N2 - 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.
AB - 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.
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U2 - 10.1038/s41564-019-0455-0
DO - 10.1038/s41564-019-0455-0
M3 - Letter
C2 - 31086313
AN - SCOPUS:85065770299
SN - 2058-5276
VL - 4
SP - 1274
EP - 1281
JO - Nature Microbiology
JF - Nature Microbiology
IS - 8
ER -