Mathematical modeling of mechanosensitive reversal control in Myxococcus xanthus

Adjusting motility patterns according to environmental cues is important for bacterial survival. Myxococcus xanthus, a bacterium moving on surfaces by gliding and twitching mechanisms, modulates the reversal frequency of its front-back polarity in response to mechanical cues like substrate stiffness...

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Main Authors: Yirui Chen, Elias J. Topo, Beiyan Nan, Jing Chen
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-01-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2023.1294631/full
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author Yirui Chen
Yirui Chen
Elias J. Topo
Beiyan Nan
Jing Chen
Jing Chen
Jing Chen
author_facet Yirui Chen
Yirui Chen
Elias J. Topo
Beiyan Nan
Jing Chen
Jing Chen
Jing Chen
author_sort Yirui Chen
collection DOAJ
description Adjusting motility patterns according to environmental cues is important for bacterial survival. Myxococcus xanthus, a bacterium moving on surfaces by gliding and twitching mechanisms, modulates the reversal frequency of its front-back polarity in response to mechanical cues like substrate stiffness and cell-cell contact. In this study, we propose that M. xanthus’s gliding machinery senses environmental mechanical cues during force generation and modulates cell reversal accordingly. To examine our hypothesis, we expand an existing mathematical model for periodic polarity reversal in M. xanthus, incorporating the experimental data on the intracellular dynamics of the gliding machinery and the interaction between the gliding machinery and a key polarity regulator. The model successfully reproduces the dependence of cell reversal frequency on substrate stiffness observed in M. xanthus gliding. We further propose reversal control networks between the gliding and twitching motility machineries to explain the opposite reversal responses observed in wild type M. xanthus cells that possess both motility mechanisms. These results provide testable predictions for future experimental investigations. In conclusion, our model suggests that the gliding machinery in M. xanthus can function as a mechanosensor, which transduces mechanical cues into a cell reversal signal.
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spelling doaj.art-0600e8dd81514a1e9b3ffd75c7fb50bf2024-01-08T20:16:53ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2024-01-011410.3389/fmicb.2023.12946311294631Mathematical modeling of mechanosensitive reversal control in Myxococcus xanthusYirui Chen0Yirui Chen1Elias J. Topo2Beiyan Nan3Jing Chen4Jing Chen5Jing Chen6Department of Biological Sciences, Virginia Tech, Blacksburg, VA, United StatesGenetics, Bioinformatics and Computational Biology Graduate Program, Virginia Tech, Blacksburg, VA, United StatesDepartment of Biology, Texas A&M University, College Station, TX, United StatesDepartment of Biology, Texas A&M University, College Station, TX, United StatesDepartment of Biological Sciences, Virginia Tech, Blacksburg, VA, United StatesFralin Life Sciences Institute, Virginia Tech, Blacksburg, VA, United StatesCenter for Soft Matter and Biological Physics, Virginia Tech, Blacksburg, VA, United StatesAdjusting motility patterns according to environmental cues is important for bacterial survival. Myxococcus xanthus, a bacterium moving on surfaces by gliding and twitching mechanisms, modulates the reversal frequency of its front-back polarity in response to mechanical cues like substrate stiffness and cell-cell contact. In this study, we propose that M. xanthus’s gliding machinery senses environmental mechanical cues during force generation and modulates cell reversal accordingly. To examine our hypothesis, we expand an existing mathematical model for periodic polarity reversal in M. xanthus, incorporating the experimental data on the intracellular dynamics of the gliding machinery and the interaction between the gliding machinery and a key polarity regulator. The model successfully reproduces the dependence of cell reversal frequency on substrate stiffness observed in M. xanthus gliding. We further propose reversal control networks between the gliding and twitching motility machineries to explain the opposite reversal responses observed in wild type M. xanthus cells that possess both motility mechanisms. These results provide testable predictions for future experimental investigations. In conclusion, our model suggests that the gliding machinery in M. xanthus can function as a mechanosensor, which transduces mechanical cues into a cell reversal signal.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1294631/fullmechanosensingbacterial motilitygliding motilitypolarity regulationmyxobacteriamathematical modeling
spellingShingle Yirui Chen
Yirui Chen
Elias J. Topo
Beiyan Nan
Jing Chen
Jing Chen
Jing Chen
Mathematical modeling of mechanosensitive reversal control in Myxococcus xanthus
Frontiers in Microbiology
mechanosensing
bacterial motility
gliding motility
polarity regulation
myxobacteria
mathematical modeling
title Mathematical modeling of mechanosensitive reversal control in Myxococcus xanthus
title_full Mathematical modeling of mechanosensitive reversal control in Myxococcus xanthus
title_fullStr Mathematical modeling of mechanosensitive reversal control in Myxococcus xanthus
title_full_unstemmed Mathematical modeling of mechanosensitive reversal control in Myxococcus xanthus
title_short Mathematical modeling of mechanosensitive reversal control in Myxococcus xanthus
title_sort mathematical modeling of mechanosensitive reversal control in myxococcus xanthus
topic mechanosensing
bacterial motility
gliding motility
polarity regulation
myxobacteria
mathematical modeling
url https://www.frontiersin.org/articles/10.3389/fmicb.2023.1294631/full
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