Literature DB >> 28655845

Force generation by groups of migrating bacteria.

Benedikt Sabass1,2, Matthias D Koch3, Guannan Liu3,4, Howard A Stone5, Joshua W Shaevitz6,4.   

Abstract

From colony formation in bacteria to wound healing and embryonic development in multicellular organisms, groups of living cells must often move collectively. Although considerable study has probed the biophysical mechanisms of how eukaryotic cells generate forces during migration, little such study has been devoted to bacteria, in particular with regard to the question of how bacteria generate and coordinate forces during collective motion. This question is addressed here using traction force microscopy. We study two distinct motility mechanisms of Myxococcus xanthus, namely, twitching and gliding. For twitching, powered by type-IV pilus retraction, we find that individual cells exert local traction in small hotspots with forces on the order of 50 pN. Twitching bacterial groups also produce traction hotspots, but with forces around 100 pN that fluctuate rapidly on timescales of <1.5 min. Gliding, the second motility mechanism, is driven by lateral transport of substrate adhesions. When cells are isolated, gliding produces low average traction on the order of 1 Pa. However, traction is amplified approximately fivefold in groups. Advancing protrusions of gliding cells push, on average, in the direction of motion. Together, these results show that the forces generated during twitching and gliding have complementary characters, and both forces have higher values when cells are in groups.

Entities:  

Keywords:  Myxococcus xanthus; bacteria; gliding; traction force; twitching

Mesh:

Substances:

Year:  2017        PMID: 28655845      PMCID: PMC5514709          DOI: 10.1073/pnas.1621469114

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  38 in total

1.  Traction fields, moments, and strain energy that cells exert on their surroundings.

Authors:  James P Butler; Iva Marija Tolić-Nørrelykke; Ben Fabry; Jeffrey J Fredberg
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Authors:  Lisa A Flanagan; Yo-El Ju; Beatrice Marg; Miriam Osterfield; Paul A Janmey
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Review 3.  How Bacteria Use Type IV Pili Machinery on Surfaces.

Authors:  Berenike Maier; Gerard C L Wong
Journal:  Trends Microbiol       Date:  2015-10-22       Impact factor: 17.079

4.  Evidence that focal adhesion complexes power bacterial gliding motility.

Authors:  Tâm Mignot; Joshua W Shaevitz; Patricia L Hartzell; David R Zusman
Journal:  Science       Date:  2007-02-09       Impact factor: 47.728

5.  Plasmodium sporozoite motility is modulated by the turnover of discrete adhesion sites.

Authors:  Sylvia Münter; Benedikt Sabass; Christine Selhuber-Unkel; Mikhail Kudryashev; Stephan Hegge; Ulrike Engel; Joachim P Spatz; Kai Matuschewski; Ulrich S Schwarz; Friedrich Frischknecht
Journal:  Cell Host Microbe       Date:  2009-12-17       Impact factor: 21.023

6.  Traction forces in locomoting cells.

Authors:  T Oliver; M Dembo; K Jacobson
Journal:  Cell Motil Cytoskeleton       Date:  1995

7.  Quantifying aggregation dynamics during Myxococcus xanthus development.

Authors:  Haiyang Zhang; Stuart Angus; Michael Tran; Chunyan Xie; Oleg A Igoshin; Roy D Welch
Journal:  J Bacteriol       Date:  2011-07-22       Impact factor: 3.490

8.  Bacterial twitching motility is coordinated by a two-dimensional tug-of-war with directional memory.

Authors:  Rahul Marathe; Claudia Meel; Nora C Schmidt; Lena Dewenter; Rainer Kurre; Lilo Greune; M Alexander Schmidt; Melanie J I Müller; Reinhard Lipowsky; Berenike Maier; Stefan Klumpp
Journal:  Nat Commun       Date:  2014-05-07       Impact factor: 14.919

9.  Contact- and Protein Transfer-Dependent Stimulation of Assembly of the Gliding Motility Machinery in Myxococcus xanthus.

Authors:  Beata Jakobczak; Daniela Keilberg; Kristin Wuichet; Lotte Søgaard-Andersen
Journal:  PLoS Genet       Date:  2015-07-01       Impact factor: 5.917

10.  The mechanism of force transmission at bacterial focal adhesion complexes.

Authors:  Laura M Faure; Jean-Bernard Fiche; Leon Espinosa; Adrien Ducret; Vivek Anantharaman; Jennifer Luciano; Sébastien Lhospice; Salim T Islam; Julie Tréguier; Mélanie Sotes; Erkin Kuru; Michael S Van Nieuwenhze; Yves V Brun; Olivier Théodoly; L Aravind; Marcelo Nollmann; Tâm Mignot
Journal:  Nature       Date:  2016-10-05       Impact factor: 49.962

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  15 in total

1.  Competitive binding of independent extension and retraction motors explains the quantitative dynamics of type IV pili.

Authors:  Matthias D Koch; Chenyi Fei; Ned S Wingreen; Joshua W Shaevitz; Zemer Gitai
Journal:  Proc Natl Acad Sci U S A       Date:  2021-02-23       Impact factor: 11.205

2.  The Interplay Between Cell-Cell and Cell-Matrix Forces Regulates Cell Migration Dynamics.

Authors:  Apratim Bajpai; Jie Tong; Weiyi Qian; Yansong Peng; Weiqiang Chen
Journal:  Biophys J       Date:  2019-10-23       Impact factor: 4.033

3.  Mechanisms for bacterial gliding motility on soft substrates.

Authors:  Joël Tchoufag; Pushpita Ghosh; Connor B Pogue; Beiyan Nan; Kranthi K Mandadapu
Journal:  Proc Natl Acad Sci U S A       Date:  2019-11-25       Impact factor: 11.205

Review 4.  Mechanomicrobiology: how bacteria sense and respond to forces.

Authors:  Yves F Dufrêne; Alexandre Persat
Journal:  Nat Rev Microbiol       Date:  2020-01-20       Impact factor: 60.633

5.  Motor Properties of PilT-Independent Type 4 Pilus Retraction in Gonococci.

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Journal:  J Bacteriol       Date:  2019-08-22       Impact factor: 3.490

6.  An In Vitro Model System to Test Mechano-Microbiological Interactions Between Bacteria and Host Cells.

Authors:  Luis Carlos Santos; Emilia Laura Munteanu; Nicolas Biais
Journal:  Methods Mol Biol       Date:  2022

7.  Flagellar Motor Transformed: Biophysical Perspectives of the Myxococcus xanthus Gliding Mechanism.

Authors:  Jing Chen; Beiyan Nan
Journal:  Front Microbiol       Date:  2022-05-06       Impact factor: 6.064

Review 8.  Materials science and mechanosensitivity of living matter.

Authors:  Alison E Patteson; Merrill E Asp; Paul A Janmey
Journal:  Appl Phys Rev       Date:  2022-03       Impact factor: 19.527

9.  Interspecies and Intraspecies Signals Synergistically Regulate Lysobacter enzymogenes Twitching Motility.

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Journal:  Appl Environ Microbiol       Date:  2019-11-14       Impact factor: 4.792

Review 10.  Type IV pili: dynamics, biophysics and functional consequences.

Authors:  Lisa Craig; Katrina T Forest; Berenike Maier
Journal:  Nat Rev Microbiol       Date:  2019-07       Impact factor: 60.633

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