Literature DB >> 27439872

Speed-dependent chemotactic precision in marine bacteria.

Kwangmin Son1, Filippo Menolascina2, Roman Stocker3.   

Abstract

Chemotaxis underpins important ecological processes in marine bacteria, from the association with primary producers to the colonization of particles and hosts. Marine bacteria often swim with a single flagellum at high speeds, alternating "runs" with either 180° reversals or ∼90° "flicks," the latter resulting from a buckling instability of the flagellum. These adaptations diverge from Escherichia coli's classic run-and-tumble motility, yet how they relate to the strong and rapid chemotaxis characteristic of marine bacteria has remained unknown. We investigated the relationship between swimming speed, run-reverse-flick motility, and high-performance chemotaxis by tracking thousands of Vibrio alginolyticus cells in microfluidic gradients. At odds with current chemotaxis models, we found that chemotactic precision-the strength of accumulation of cells at the peak of a gradient-is swimming-speed dependent in V. alginolyticus Faster cells accumulate twofold more tightly by chemotaxis compared with slower cells, attaining an advantage in the exploitation of a resource additional to that of faster gradient climbing. Trajectory analysis and an agent-based mathematical model revealed that this unexpected advantage originates from a speed dependence of reorientation frequency and flicking, which were higher for faster cells, and was compounded by chemokinesis, an increase in speed with resource concentration. The absence of any one of these adaptations led to a 65-70% reduction in the population-level resource exposure. These findings indicate that, contrary to what occurs in E. coli, swimming speed can be a fundamental determinant of the gradient-seeking capabilities of marine bacteria, and suggest a new model of bacterial chemotaxis.

Entities:  

Keywords:  chemokinesis; chemotaxis; motility; ocean; run–reverse–flick

Mesh:

Year:  2016        PMID: 27439872      PMCID: PMC4978249          DOI: 10.1073/pnas.1602307113

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


  23 in total

1.  A sensitive, versatile microfluidic assay for bacterial chemotaxis.

Authors:  Hanbin Mao; Paul S Cremer; Michael D Manson
Journal:  Proc Natl Acad Sci U S A       Date:  2003-04-18       Impact factor: 11.205

2.  MOTILE MARINE BACTERIA. I. TECHNIQUES, ECOLOGY, AND GENERAL CHARACTERISTICS.

Authors:  E LEIFSON; B J COSENZA; R MURCHELANO; R C CLEVERDON
Journal:  J Bacteriol       Date:  1964-03       Impact factor: 3.490

3.  Chemotaxis toward phytoplankton drives organic matter partitioning among marine bacteria.

Authors:  Steven Smriga; Vicente I Fernandez; James G Mitchell; Roman Stocker
Journal:  Proc Natl Acad Sci U S A       Date:  2016-01-22       Impact factor: 11.205

4.  Experimental verification of the behavioral foundation of bacterial transport parameters using microfluidics.

Authors:  Tanvir Ahmed; Roman Stocker
Journal:  Biophys J       Date:  2008-07-25       Impact factor: 4.033

5.  Dynamics of mechanosensing in the bacterial flagellar motor.

Authors:  Pushkar P Lele; Basarab G Hosu; Howard C Berg
Journal:  Proc Natl Acad Sci U S A       Date:  2013-07-01       Impact factor: 11.205

6.  Bacterial tracking of motile algae.

Authors:  Greg M Barbara; James G Mitchell
Journal:  FEMS Microbiol Ecol       Date:  2003-05-01       Impact factor: 4.194

7.  Response rescaling in bacterial chemotaxis.

Authors:  Milena D Lazova; Tanvir Ahmed; Domenico Bellomo; Roman Stocker; Thomas S Shimizu
Journal:  Proc Natl Acad Sci U S A       Date:  2011-08-01       Impact factor: 11.205

8.  Quantitative modeling of Escherichia coli chemotactic motion in environments varying in space and time.

Authors:  Lili Jiang; Qi Ouyang; Yuhai Tu
Journal:  PLoS Comput Biol       Date:  2010-04-08       Impact factor: 4.475

9.  Rapid chemotactic response enables marine bacteria to exploit ephemeral microscale nutrient patches.

Authors:  Roman Stocker; Justin R Seymour; Azadeh Samadani; Dana E Hunt; Martin F Polz
Journal:  Proc Natl Acad Sci U S A       Date:  2008-03-12       Impact factor: 11.205

10.  The sodium-driven polar flagellar motor of marine Vibrio as the mechanosensor that regulates lateral flagellar expression.

Authors:  I Kawagishi; M Imagawa; Y Imae; L McCarter; M Homma
Journal:  Mol Microbiol       Date:  1996-05       Impact factor: 3.501

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  26 in total

Review 1.  Zooming in on the phycosphere: the ecological interface for phytoplankton-bacteria relationships.

Authors:  Justin R Seymour; Shady A Amin; Jean-Baptiste Raina; Roman Stocker
Journal:  Nat Microbiol       Date:  2017-05-30       Impact factor: 17.745

Review 2.  Biophysical methods to quantify bacterial behaviors at oil-water interfaces.

Authors:  Jacinta C Conrad
Journal:  J Ind Microbiol Biotechnol       Date:  2020-08-02       Impact factor: 3.346

3.  Particle foraging strategies promote microbial diversity in marine environments.

Authors:  Ali Ebrahimi; Akshit Goyal; Otto X Cordero
Journal:  Elife       Date:  2022-03-15       Impact factor: 8.140

4.  Chemotaxis may assist marine heterotrophic bacterial diazotrophs to find microzones suitable for N2 fixation in the pelagic ocean.

Authors:  Søren Hallstrøm; Jean-Baptiste Raina; Martin Ostrowski; Donovan H Parks; Gene W Tyson; Philip Hugenholtz; Roman Stocker; Justin R Seymour; Lasse Riemann
Journal:  ISME J       Date:  2022-08-01       Impact factor: 11.217

5.  Steady-state running rate sets the speed and accuracy of accumulation of swimming bacteria.

Authors:  Margaritis Voliotis; Jerko Rosko; Teuta Pilizota; Tanniemola B Liverpool
Journal:  Biophys J       Date:  2022-08-31       Impact factor: 3.699

6.  Vibrio cholerae Type VI Activity Alters Motility Behavior in Mucin.

Authors:  Abby Frederick; Yuhsun Huang; Meng Pu; Dean A Rowe-Magnus
Journal:  J Bacteriol       Date:  2020-11-19       Impact factor: 3.490

Review 7.  The role of microbial motility and chemotaxis in symbiosis.

Authors:  Jean-Baptiste Raina; Vicente Fernandez; Bennett Lambert; Roman Stocker; Justin R Seymour
Journal:  Nat Rev Microbiol       Date:  2019-05       Impact factor: 60.633

8.  Collective motion enhances chemotaxis in a two-dimensional bacterial swarm.

Authors:  Maojin Tian; Chi Zhang; Rongjing Zhang; Junhua Yuan
Journal:  Biophys J       Date:  2021-02-23       Impact factor: 4.033

9.  Host-emitted amino acid cues regulate bacterial chemokinesis to enhance colonization.

Authors:  Catherine D Robinson; Emily G Sweeney; Julia Ngo; Emily Ma; Arden Perkins; T Jarrod Smith; Nicolas L Fernandez; Christopher M Waters; S James Remington; Brendan J M Bohannan; Karen Guillemin
Journal:  Cell Host Microbe       Date:  2021-07-06       Impact factor: 31.316

10.  The Stand-Alone PilZ-Domain Protein MotL Specifically Regulates the Activity of the Secondary Lateral Flagellar System in Shewanella putrefaciens.

Authors:  Anna Pecina; Meike Schwan; Vitan Blagotinsek; Tim Rick; Patrick Klüber; Tabea Leonhard; Gert Bange; Kai M Thormann
Journal:  Front Microbiol       Date:  2021-06-01       Impact factor: 5.640

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