Literature DB >> 25296304

Uncovering the mechanism of trapping and cell orientation during Neisseria gonorrhoeae twitching motility.

Vasily Zaburdaev1, Nicolas Biais2, Michael Schmiedeberg3, Jens Eriksson4, Ann-Beth Jonsson5, Michael P Sheetz6, David A Weitz7.   

Abstract

Neisseria gonorrheae bacteria are the causative agent of the second most common sexually transmitted infection in the world. The bacteria move on a surface by means of twitching motility. Their movement is mediated by multiple long and flexible filaments, called type IV pili, that extend from the cell body, attach to the surface, and retract, thus generating a pulling force. Moving cells also use pili to aggregate and form microcolonies. However, the mechanism by which the pili surrounding the cell body work together to propel bacteria remains unclear. Understanding this process will help describe the motility of N. gonorrheae bacteria, and thus the dissemination of the disease which they cause. In this article we track individual twitching cells and observe that their trajectories consist of alternating moving and pausing intervals, while the cell body is preferably oriented with its wide side toward the direction of motion. Based on these data, we propose a model for the collective pili operation of N. gonorrheae bacteria that explains the experimentally observed behavior. Individual pili function independently but can lead to coordinated motion or pausing via the force balance. The geometry of the cell defines its orientation during motion. We show that by changing pili substrate interactions, the motility pattern can be altered in a predictable way. Although the model proposed is tangibly simple, it still has sufficient robustness to incorporate further advanced pili features and various cell geometries to describe other bacteria that employ pili to move on surfaces.
Copyright © 2014 Biophysical Society. Published by Elsevier Inc. All rights reserved.

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Year:  2014        PMID: 25296304      PMCID: PMC4190650          DOI: 10.1016/j.bpj.2014.07.061

Source DB:  PubMed          Journal:  Biophys J        ISSN: 0006-3495            Impact factor:   4.033


  26 in total

1.  Direct observation of extension and retraction of type IV pili.

Authors:  J M Skerker; H C Berg
Journal:  Proc Natl Acad Sci U S A       Date:  2001-05-29       Impact factor: 11.205

Review 2.  Bacterial biofilms: a common cause of persistent infections.

Authors:  J W Costerton; P S Stewart; E P Greenberg
Journal:  Science       Date:  1999-05-21       Impact factor: 47.728

3.  Single pilus motor forces exceed 100 pN.

Authors:  Berenike Maier; Laura Potter; Magdalene So; Cynthia D Long; Hank S Seifert; Michael P Sheetz
Journal:  Proc Natl Acad Sci U S A       Date:  2002-11-22       Impact factor: 11.205

Review 4.  Type IV pili and twitching motility.

Authors:  John S Mattick
Journal:  Annu Rev Microbiol       Date:  2002-01-30       Impact factor: 15.500

5.  The Che4 pathway of Myxococcus xanthus regulates type IV pilus-mediated motility.

Authors:  Hera C Vlamakis; John R Kirby; David R Zusman
Journal:  Mol Microbiol       Date:  2004-06       Impact factor: 3.501

Review 6.  Bacterial biofilms: from the natural environment to infectious diseases.

Authors:  Luanne Hall-Stoodley; J William Costerton; Paul Stoodley
Journal:  Nat Rev Microbiol       Date:  2004-02       Impact factor: 60.633

7.  Pilus retraction powers bacterial twitching motility.

Authors:  A J Merz; M So; M P Sheetz
Journal:  Nature       Date:  2000-09-07       Impact factor: 49.962

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.  Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development.

Authors:  G A O'Toole; R Kolter
Journal:  Mol Microbiol       Date:  1998-10       Impact factor: 3.501

10.  Studies on gonococcus infection. I. Pili and zones of adhesion: their relation to gonococcal growth patterns.

Authors:  J Swanson; S J Kraus; E C Gotschlich
Journal:  J Exp Med       Date:  1971-10-01       Impact factor: 14.307

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  13 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.  Comparative Analysis of Type IV Pilin in Desulfuromonadales.

Authors:  Chuanjun Shu; Ke Xiao; Qin Yan; Xiao Sun
Journal:  Front Microbiol       Date:  2016-12-21       Impact factor: 5.640

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

Authors:  Robert Zöllner; Tom Cronenberg; Berenike Maier
Journal:  J Bacteriol       Date:  2019-08-22       Impact factor: 3.490

Review 4.  Staying in Shape: the Impact of Cell Shape on Bacterial Survival in Diverse Environments.

Authors:  Desirée C Yang; Kris M Blair; Nina R Salama
Journal:  Microbiol Mol Biol Rev       Date:  2016-02-10       Impact factor: 11.056

5.  Role of Cyclic Di-GMP and Exopolysaccharide in Type IV Pilus Dynamics.

Authors:  Jan Ribbe; Amy E Baker; Sebastian Euler; George A O'Toole; Berenike Maier
Journal:  J Bacteriol       Date:  2017-03-28       Impact factor: 3.490

6.  Perturbing the acetylation status of the Type IV pilus retraction motor, PilT, reduces Neisseria gonorrhoeae viability.

Authors:  Alyson M Hockenberry; Deborah M B Post; Katherine A Rhodes; Michael Apicella; Magdalene So
Journal:  Mol Microbiol       Date:  2018-10-28       Impact factor: 3.501

Review 7.  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

8.  Kingella kingae PilC1 and PilC2 are adhesive multifunctional proteins that promote bacterial adherence, twitching motility, DNA transformation, and pilus biogenesis.

Authors:  Alexandra L Sacharok; Eric A Porsch; Taylor A Yount; Orlaith Keenan; Joseph W St Geme
Journal:  PLoS Pathog       Date:  2022-03-30       Impact factor: 6.823

9.  Pili-Induced Clustering of N. gonorrhoeae Bacteria.

Authors:  Johannes Taktikos; Yen Ting Lin; Holger Stark; Nicolas Biais; Vasily Zaburdaev
Journal:  PLoS One       Date:  2015-09-10       Impact factor: 3.240

10.  Inoculation density and nutrient level determine the formation of mushroom-shaped structures in Pseudomonas aeruginosa biofilms.

Authors:  Azadeh Ghanbari; Jaber Dehghany; Timo Schwebs; Mathias Müsken; Susanne Häussler; Michael Meyer-Hermann
Journal:  Sci Rep       Date:  2016-09-09       Impact factor: 4.379

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