Literature DB >> 33927052

Large-Scale Vortices with Dynamic Rotation Emerged from Monolayer Collective Motion of Gliding Flavobacteria.

Daisuke Nakane1, Shoko Odaka2, Kana Suzuki2, Takayuki Nishizaka2.   

Abstract

A collective motion of self-driven particles has been a fascinating subject in physics and biology. Sophisticated macroscopic behavior emerges through a population of thousands or millions of bacterial cells propelling itself by flagellar rotation and chemotactic responses. Here, we found a series of collective motions accompanying successive phase transitions for a nonflagellated rod-shaped soil bacterium, Flavobacterium johnsoniae, which was driven by a surface cell movement known as gliding motility. When we spotted the cells on an agar plate with a low level of nutrients, the bacterial community exhibited vortex patterns that spontaneously appeared as lattice and integrated into a large-scale circular plate. All patterns were exhibited with a monolayer of bacteria, which enabled us to two-dimensionally visualize an individual cell with high resolution within a wide-range pattern. The single cells moved with random orientation, but the cells that were connected with one another showed left-turn-biased trajectories in a starved environment. This feature is possibly due to the collision of cells inducing a nematic alignment of dense cells as self-propelled rods. Subsequently, each vortex oscillated independently and then transformed to the rotating mode as an independent circular plate. Notably, the rotational direction of the circular plate was counterclockwise without exception. The plates developed accompanying rotation with constant angular velocity, suggesting that the mode is an efficient strategy for bacterial survival. IMPORTANCE Self-propelled bacteria propelled by flagellar rotation often display highly organized dynamic patterns at high cell densities. Here, we found a new mode of collective motion in nonflagellated bacteria; vortex patterns spontaneously appeared as lattice and were integrated into a large-scale circular plate, comprising hundreds of thousands of cells, which exhibited unidirectional rotation in a counterclockwise manner and expanded in size on agar. A series of collective motions was driven by gliding motility of the rod-shaped soil bacterium Flavobacterium johnsoniae. In a low-nutrient environment, single cells moved with random orientation, while cells at high density moved together as a unitary cluster. This might be an efficient strategy for cells of this species to find nutrients.

Entities:  

Keywords:  colony patterns; flavobacterium; motility; signal transduction; starvation; video microscopy

Mesh:

Year:  2021        PMID: 33927052      PMCID: PMC8223929          DOI: 10.1128/JB.00073-21

Source DB:  PubMed          Journal:  J Bacteriol        ISSN: 0021-9193            Impact factor:   3.490


  37 in total

1.  Cell behavior in traveling wave patterns of myxobacteria.

Authors:  R Welch; D Kaiser
Journal:  Proc Natl Acad Sci U S A       Date:  2001-12-18       Impact factor: 11.205

2.  Cooperative formation of chiral patterns during growth of bacterial colonies.

Authors: 
Journal:  Phys Rev Lett       Date:  1995-10-09       Impact factor: 9.161

3.  Transmission of a signal that synchronizes cell movements in swarms of Myxococcus xanthus.

Authors:  Dale Kaiser; Hans Warrick
Journal:  Proc Natl Acad Sci U S A       Date:  2014-08-22       Impact factor: 11.205

Review 4.  Biofilms: an emergent form of bacterial life.

Authors:  Hans-Curt Flemming; Jost Wingender; Ulrich Szewzyk; Peter Steinberg; Scott A Rice; Staffan Kjelleberg
Journal:  Nat Rev Microbiol       Date:  2016-08-11       Impact factor: 60.633

5.  Generic modelling of cooperative growth patterns in bacterial colonies.

Authors:  E Ben-Jacob; O Schochet; A Tenenbaum; I Cohen; A Czirók; T Vicsek
Journal:  Nature       Date:  1994-03-03       Impact factor: 49.962

Review 6.  From individual cell motility to collective behaviors: insights from a prokaryote, Myxococcus xanthus.

Authors:  Yong Zhang; Adrien Ducret; Joshua Shaevitz; Tâm Mignot
Journal:  FEMS Microbiol Rev       Date:  2011-10-03       Impact factor: 16.408

7.  Novel features of the polysaccharide-digesting gliding bacterium Flavobacterium johnsoniae as revealed by genome sequence analysis.

Authors:  Mark J McBride; Gary Xie; Eric C Martens; Alla Lapidus; Bernard Henrissat; Ryan G Rhodes; Eugene Goltsman; Wei Wang; Jian Xu; David W Hunnicutt; Andrew M Staroscik; Timothy R Hoover; Yi-Qiang Cheng; Jennifer L Stein
Journal:  Appl Environ Microbiol       Date:  2009-08-28       Impact factor: 4.792

8.  Swarming bacteria migrate by Lévy Walk.

Authors:  Gil Ariel; Amit Rabani; Sivan Benisty; Jonathan D Partridge; Rasika M Harshey; Avraham Be'er
Journal:  Nat Commun       Date:  2015-09-25       Impact factor: 14.919

9.  From cell differentiation to cell collectives: Bacillus subtilis uses division of labor to migrate.

Authors:  Jordi van Gestel; Hera Vlamakis; Roberto Kolter
Journal:  PLoS Biol       Date:  2015-04-20       Impact factor: 8.029

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  1 in total

Review 1.  Design Principles of the Rotary Type 9 Secretion System.

Authors:  Abhishek Trivedi; Jitendrapuri Gosai; Daisuke Nakane; Abhishek Shrivastava
Journal:  Front Microbiol       Date:  2022-05-10       Impact factor: 6.064

  1 in total

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