Literature DB >> 19580745

A mechanism for precision-sensing via a gradient-sensing pathway: a model of Escherichia coli thermotaxis.

Lili Jiang1, Qi Ouyang, Yuhai Tu.   

Abstract

Thermotaxis is the phenomenon where an organism directs its movement toward its preferred temperature. So far, the molecular origin for this precision-sensing behavior remains a puzzle. We propose a model of Escherichia coli thermotaxis and show that the precision-sensing behavior in E. coli thermotaxis can be carried out by the gradient-sensing chemotaxis pathway under two general conditions. First, the thermosensor response to temperature is inverted by its internal adaptation state. For E. coli, chemoreceptor Tar changes from a warm sensor to a cold sensor on increase of its methylation level. Second, temperature directly affects the adaptation kinetics. The adapted activity in E. coli increases with temperature in contrast to the perfect adaptation to chemical stimuli. Given these two conditions, E. coli thermotaxis is achieved by the cryophilic and thermophilic responses for temperature above and below a critical temperature Tc, which is encoded by internal pathway parameters. Our model results are supported by both experiments with adaptation-disabled mutants and the recent temperature impulse response measurements for wild-type cells. Tc is predicted to decrease with the background attractant concentration. This mechanism for precision sensing in an adaptive gradient-sensing system may apply to other organisms, such as Dictyostelium discoideum and Caenorhabditis elegans.

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Year:  2009        PMID: 19580745      PMCID: PMC2711378          DOI: 10.1016/j.bpj.2009.04.029

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


  27 in total

1.  Perfect and near-perfect adaptation in a model of bacterial chemotaxis.

Authors:  Bernardo A Mello; Yuhai Tu
Journal:  Biophys J       Date:  2003-05       Impact factor: 4.033

2.  Normal and mutant thermotaxis in the nematode Caenorhabditis elegans.

Authors:  E M Hedgecock; R L Russell
Journal:  Proc Natl Acad Sci U S A       Date:  1975-10       Impact factor: 11.205

3.  An allosteric model for heterogeneous receptor complexes: understanding bacterial chemotaxis responses to multiple stimuli.

Authors:  Bernardo A Mello; Yuhai Tu
Journal:  Proc Natl Acad Sci U S A       Date:  2005-11-17       Impact factor: 11.205

Review 4.  Signal transduction in bacterial chemotaxis.

Authors:  Melinda D Baker; Peter M Wolanin; Jeffry B Stock
Journal:  Bioessays       Date:  2006-01       Impact factor: 4.345

5.  Chemosensing in Escherichia coli: two regimes of two-state receptors.

Authors:  Juan E Keymer; Robert G Endres; Monica Skoge; Yigal Meir; Ned S Wingreen
Journal:  Proc Natl Acad Sci U S A       Date:  2006-01-30       Impact factor: 11.205

6.  Monitoring bacterial chemotaxis by using bioluminescence resonance energy transfer: absence of feedback from the flagellar motors.

Authors:  Thomas S Shimizu; Nicolas Delalez; Klemens Pichler; Howard C Berg
Journal:  Proc Natl Acad Sci U S A       Date:  2006-02-01       Impact factor: 11.205

Review 7.  Bacterial chemoreceptors: high-performance signaling in networked arrays.

Authors:  Gerald L Hazelbauer; Joseph J Falke; John S Parkinson
Journal:  Trends Biochem Sci       Date:  2007-12-31       Impact factor: 13.807

8.  Robustness in bacterial chemotaxis.

Authors:  U Alon; M G Surette; N Barkai; S Leibler
Journal:  Nature       Date:  1999-01-14       Impact factor: 49.962

9.  Robustness in simple biochemical networks.

Authors:  N Barkai; S Leibler
Journal:  Nature       Date:  1997-06-26       Impact factor: 49.962

10.  Thermosensing properties of mutant aspartate chemoreceptors with methyl-accepting sites replaced singly or multiply by alanine.

Authors:  S Nishiyama; T Nara; M Homma; Y Imae; I Kawagishi
Journal:  J Bacteriol       Date:  1997-11       Impact factor: 3.490

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  8 in total

1.  Optogenetic Manipulation of Cyclic Di-GMP (c-di-GMP) Levels Reveals the Role of c-di-GMP in Regulating Aerotaxis Receptor Activity in Azospirillum brasilense.

Authors:  Lindsey O'Neal; Min-Hyung Ryu; Mark Gomelsky; Gladys Alexandre
Journal:  J Bacteriol       Date:  2017-08-22       Impact factor: 3.490

2.  Thermal robustness of signaling in bacterial chemotaxis.

Authors:  Olga Oleksiuk; Vladimir Jakovljevic; Nikita Vladimirov; Ricardo Carvalho; Eli Paster; William S Ryu; Yigal Meir; Ned S Wingreen; Markus Kollmann; Victor Sourjik
Journal:  Cell       Date:  2011-04-15       Impact factor: 41.582

3.  Precision sensing by two opposing gradient sensors: how does Escherichia coli find its preferred pH level?

Authors:  Bo Hu; Yuhai Tu
Journal:  Biophys J       Date:  2013-07-02       Impact factor: 4.033

4.  Precision and variability in bacterial temperature sensing.

Authors:  Anna Yoney; Hanna Salman
Journal:  Biophys J       Date:  2015-05-19       Impact factor: 4.033

Review 5.  Quantitative modeling of bacterial chemotaxis: signal amplification and accurate adaptation.

Authors:  Yuhai Tu
Journal:  Annu Rev Biophys       Date:  2013-02-28       Impact factor: 12.981

6.  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

7.  Mechanism of bidirectional thermotaxis in Escherichia coli.

Authors:  Anja Paulick; Vladimir Jakovljevic; SiMing Zhang; Michael Erickstad; Alex Groisman; Yigal Meir; William S Ryu; Ned S Wingreen; Victor Sourjik
Journal:  Elife       Date:  2017-08-03       Impact factor: 8.140

8.  Behaviors and strategies of bacterial navigation in chemical and nonchemical gradients.

Authors:  Bo Hu; Yuhai Tu
Journal:  PLoS Comput Biol       Date:  2014-06-19       Impact factor: 4.475

  8 in total

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