Literature DB >> 31097577

Bacteria push the limits of chemotactic precision to navigate dynamic chemical gradients.

Douglas R Brumley1, Francesco Carrara2, Andrew M Hein3, Yutaka Yawata4,5, Simon A Levin6, Roman Stocker2.   

Abstract

Ephemeral aggregations of bacteria are ubiquitous in the environment, where they serve as hotbeds of metabolic activity, nutrient cycling, and horizontal gene transfer. In many cases, these regions of high bacterial concentration are thought to form when motile cells use chemotaxis to navigate to chemical hotspots. However, what governs the dynamics of bacterial aggregations is unclear. Here, we use an experimental platform to create realistic submillimeter-scale nutrient pulses with controlled nutrient concentrations. By combining experiments, mathematical theory, and agent-based simulations, we show that individual Vibrio ordalii bacteria begin chemotaxis toward hotspots of dissolved organic matter (DOM) when the magnitude of the chemical gradient rises sufficiently far above the sensory noise that is generated by stochastic encounters with chemoattractant molecules. Each DOM hotspot is surrounded by a dynamic ring of chemotaxing cells, which congregate in regions of high DOM concentration before dispersing as DOM diffuses and gradients become too noisy for cells to respond to. We demonstrate that V. ordalii operates close to the theoretical limits on chemotactic precision. Numerical simulations of chemotactic bacteria, in which molecule counting noise is explicitly taken into account, point at a tradeoff between nutrient acquisition and the cost of chemotactic precision. More generally, our results illustrate how limits on sensory precision can be used to understand the location, spatial extent, and lifespan of bacterial behavioral responses in ecologically relevant environments.

Entities:  

Keywords:  chemotaxis; microbial ecology; motility; ocean; sensing noise

Year:  2019        PMID: 31097577      PMCID: PMC6561191          DOI: 10.1073/pnas.1816621116

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


  44 in total

1.  An ultrasensitive bacterial motor revealed by monitoring signaling proteins in single cells.

Authors:  P Cluzel; M Surette; S Leibler
Journal:  Science       Date:  2000-03-03       Impact factor: 47.728

2.  Binding of the Escherichia coli response regulator CheY to its target measured in vivo by fluorescence resonance energy transfer.

Authors:  Victor Sourjik; Howard C Berg
Journal:  Proc Natl Acad Sci U S A       Date:  2002-09-13       Impact factor: 11.205

3.  From molecular noise to behavioural variability in a single bacterium.

Authors:  Ekaterina Korobkova; Thierry Emonet; Jose M G Vilar; Thomas S Shimizu; Philippe Cluzel
Journal:  Nature       Date:  2004-04-01       Impact factor: 49.962

4.  A free-energy-based stochastic simulation of the Tar receptor complex.

Authors:  C J Morton-Firth; T S Shimizu; D Bray
Journal:  J Mol Biol       Date:  1999-03-05       Impact factor: 5.469

Review 5.  Making sense of it all: bacterial chemotaxis.

Authors:  George H Wadhams; Judith P Armitage
Journal:  Nat Rev Mol Cell Biol       Date:  2004-12       Impact factor: 94.444

6.  Physical limits to biochemical signaling.

Authors:  William Bialek; Sima Setayeshgar
Journal:  Proc Natl Acad Sci U S A       Date:  2005-07-08       Impact factor: 11.205

7.  The chemotactic behavior of computer-based surrogate bacteria.

Authors:  Dennis Bray; Matthew D Levin; Karen Lipkow
Journal:  Curr Biol       Date:  2007-01-09       Impact factor: 10.834

Review 8.  Microbial structuring of marine ecosystems.

Authors:  Farooq Azam; Francesca Malfatti
Journal:  Nat Rev Microbiol       Date:  2007-10       Impact factor: 60.633

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.  Accuracy of direct gradient sensing by single cells.

Authors:  Robert G Endres; Ned S Wingreen
Journal:  Proc Natl Acad Sci U S A       Date:  2008-10-08       Impact factor: 11.205

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  11 in total

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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

2.  Random encounters and amoeba locomotion drive the predation of Listeria monocytogenes by Acanthamoeba castellanii.

Authors:  Frédéric de Schaetzen; Mingzhen Fan; Uria Alcolombri; François J Peaudecerf; David Drissner; Martin J Loessner; Roman Stocker; Markus Schuppler
Journal:  Proc Natl Acad Sci U S A       Date:  2022-08-01       Impact factor: 12.779

Review 3.  The ecological roles of bacterial chemotaxis.

Authors:  Johannes M Keegstra; Francesco Carrara; Roman Stocker
Journal:  Nat Rev Microbiol       Date:  2022-03-15       Impact factor: 78.297

4.  Chemotaxis shapes the microscale organization of the ocean's microbiome.

Authors:  Jean-Baptiste Raina; Bennett S Lambert; Donovan H Parks; Christian Rinke; Nachshon Siboni; Anna Bramucci; Martin Ostrowski; Brandon Signal; Adrian Lutz; Himasha Mendis; Francesco Rubino; Vicente I Fernandez; Roman Stocker; Philip Hugenholtz; Gene W Tyson; Justin R Seymour
Journal:  Nature       Date:  2022-04-20       Impact factor: 69.504

5.  Wnt- and glutamate-receptors orchestrate stem cell dynamics and asymmetric cell division.

Authors:  Sergi Junyent; Joshua C Reeves; James LA Szczerkowski; Clare L Garcin; Tung-Jui Trieu; Matthew Wilson; Jethro Lundie-Brown; Shukry J Habib
Journal:  Elife       Date:  2021-05-24       Impact factor: 8.140

6.  A Multi-Scale Approach to Modeling E. coli Chemotaxis.

Authors:  Eran Agmon; Ryan K Spangler
Journal:  Entropy (Basel)       Date:  2020-09-29       Impact factor: 2.524

7.  The Genomic Capabilities of Microbial Communities Track Seasonal Variation in Environmental Conditions of Arctic Lagoons.

Authors:  Kristina D Baker; Colleen T E Kellogg; James W McClelland; Kenneth H Dunton; Byron C Crump
Journal:  Front Microbiol       Date:  2021-02-12       Impact factor: 5.640

8.  Chemokinesis-driven accumulation of active colloids in low-mobility regions of fuel gradients.

Authors:  Jeffrey L Moran; Philip M Wheat; Nathan A Marine; Jonathan D Posner
Journal:  Sci Rep       Date:  2021-02-26       Impact factor: 4.379

9.  Migration and accumulation of bacteria with chemotaxis and chemokinesis.

Authors:  Theresa Jakuszeit; James Lindsey-Jones; François J Peaudecerf; Ottavio A Croze
Journal:  Eur Phys J E Soft Matter       Date:  2021-03-15       Impact factor: 1.890

Review 10.  Evolution of glutamatergic signaling and synapses.

Authors:  Leonid L Moroz; Mikhail A Nikitin; Pavlin G Poličar; Andrea B Kohn; Daria Y Romanova
Journal:  Neuropharmacology       Date:  2021-07-31       Impact factor: 5.273

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