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Title: Mechanisms for bacterial gliding motility on soft substrates

Abstract

The motility mechanism of certain prokaryotes has long been a mystery, since their motion, known as gliding, involves no external appendages. The physical principles behind gliding still remain poorly understood. Using myxobacteria as an example of such organisms, we identify here the physical principles behind gliding motility and develop a theoretical model that predicts a 2-regime behavior of the gliding speed as a function of the substrate stiffness. Our theory describes the elasto-capillary–hydrodynamic interactions between the membrane of the bacteria, the slime it secretes, and the soft substrate underneath. Defining gliding as the horizontal translation under zero net force, we find the 2-regime behavior is due to 2 distinct mechanisms of motility thrust. On mildly soft substrates, the thrust arises from bacterial shape deformations creating a flow of slime that exerts a pressure along the bacterial length. This pressure in conjunction with the bacterial shape provides the necessary thrust for propulsion. On very soft substrates, however, we show that capillary effects must be considered that lead to the formation of a ridge at the slime–substrate–air interface, thereby creating a thrust in the form of a localized pressure gradient at the bacterial leading edge. To test our theory, we perform experimentsmore » with isolated cells on agar substrates of varying stiffness and find the measured gliding speeds in good agreement with the predictions from our elasto-capillary–hydrodynamic model. Finally, the mechanisms reported here serve as an important step toward an accurate theory of friction and substrate-mediated interactions between bacteria proliferating in soft media.« less

Authors:
 [1]; ORCiD logo [2];  [3]; ORCiD logo [3];  [4]
  1. Univ. of California, Berkeley, CA (United States)
  2. Tata Inst. of Fundamental Research, Hyderabad (India)
  3. Texas A & M Univ., College Station, TX (United States)
  4. Univ. of California, Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC); National Institutes of Health (NIH)
OSTI Identifier:
1603549
Grant/Contract Number:  
AC02-05CH11231; R01-GM110066
Resource Type:
Accepted Manuscript
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 116; Journal Issue: 50; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; myxobacteria; gliding motility; mechanosensitivity; lubrication; elasto-capillary-hydrodynamics

Citation Formats

Tchoufag, Joël, Ghosh, Pushpita, Pogue, Connor B., Nan, Beiyan, and Mandadapu, Kranthi K. Mechanisms for bacterial gliding motility on soft substrates. United States: N. p., 2019. Web. doi:10.1073/pnas.1914678116.
Tchoufag, Joël, Ghosh, Pushpita, Pogue, Connor B., Nan, Beiyan, & Mandadapu, Kranthi K. Mechanisms for bacterial gliding motility on soft substrates. United States. doi:https://doi.org/10.1073/pnas.1914678116
Tchoufag, Joël, Ghosh, Pushpita, Pogue, Connor B., Nan, Beiyan, and Mandadapu, Kranthi K. Mon . "Mechanisms for bacterial gliding motility on soft substrates". United States. doi:https://doi.org/10.1073/pnas.1914678116. https://www.osti.gov/servlets/purl/1603549.
@article{osti_1603549,
title = {Mechanisms for bacterial gliding motility on soft substrates},
author = {Tchoufag, Joël and Ghosh, Pushpita and Pogue, Connor B. and Nan, Beiyan and Mandadapu, Kranthi K.},
abstractNote = {The motility mechanism of certain prokaryotes has long been a mystery, since their motion, known as gliding, involves no external appendages. The physical principles behind gliding still remain poorly understood. Using myxobacteria as an example of such organisms, we identify here the physical principles behind gliding motility and develop a theoretical model that predicts a 2-regime behavior of the gliding speed as a function of the substrate stiffness. Our theory describes the elasto-capillary–hydrodynamic interactions between the membrane of the bacteria, the slime it secretes, and the soft substrate underneath. Defining gliding as the horizontal translation under zero net force, we find the 2-regime behavior is due to 2 distinct mechanisms of motility thrust. On mildly soft substrates, the thrust arises from bacterial shape deformations creating a flow of slime that exerts a pressure along the bacterial length. This pressure in conjunction with the bacterial shape provides the necessary thrust for propulsion. On very soft substrates, however, we show that capillary effects must be considered that lead to the formation of a ridge at the slime–substrate–air interface, thereby creating a thrust in the form of a localized pressure gradient at the bacterial leading edge. To test our theory, we perform experiments with isolated cells on agar substrates of varying stiffness and find the measured gliding speeds in good agreement with the predictions from our elasto-capillary–hydrodynamic model. Finally, the mechanisms reported here serve as an important step toward an accurate theory of friction and substrate-mediated interactions between bacteria proliferating in soft media.},
doi = {10.1073/pnas.1914678116},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 50,
volume = 116,
place = {United States},
year = {2019},
month = {11}
}

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