Escherichia coli swimming is robust against variations in flagellar number

Bacterial chemotaxis is a paradigm for how environmental signals modulate cellular behavior. Although the network underlying this process has been studied extensively, we do not yet have an end-to-end understanding of chemotaxis. Specifically, how the rotational states of a cell’s flagella cooperatively determine whether the cell ‘runs’ or ‘tumbles’ remains poorly characterized. Here, we measure the swimming behavior of individual E. coli cells while simultaneously detecting the rotational states of each flagellum. We find that a simple mathematical expression relates the cell’s run/tumble bias to the number and average rotational state of its flagella. However, due to inter-flagellar correlations, an ‘effective number’ of flagella—smaller than the actual number—enters into this relation. Data from a chemotaxis mutant and stochastic modeling suggest that fluctuations of the regulator CheY-P are the source of flagellar correlations. A consequence of inter-flagellar correlations is that run/tumble behavior is only weakly dependent on number of flagella. DOI: http://dx.doi.org/10.7554/eLife.01916.001

[1]  Thierry Emonet,et al.  Stochastic coordination of multiple actuators reduces latency and improves chemotactic response in bacteria , 2011, Proceedings of the National Academy of Sciences.

[2]  S. Leibler,et al.  An ultrasensitive bacterial motor revealed by monitoring signaling proteins in single cells. , 2000, Science.

[3]  B. Wanner,et al.  One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[4]  Nikita Vladimirov,et al.  Dependence of Bacterial Chemotaxis on Gradient Shape and Adaptation Rate , 2008, PLoS Comput. Biol..

[5]  T. Ha,et al.  Ultrahigh-resolution optical trap with single-fluorophore sensitivity , 2011, Nature Methods.

[6]  Dennis Bray,et al.  The Chemotactic Behavior of Computer-Based Surrogate Bacteria , 2007, Current Biology.

[7]  H. Berg,et al.  Impulse responses in bacterial chemotaxis , 1982, Cell.

[8]  Eyal Shimoni,et al.  The bacterial flagellar switch complex is getting more complex , 2008, The EMBO journal.

[9]  R M Macnab,et al.  Normal-to-curly flagellar transitions and their role in bacterial tumbling. Stabilization of an alternative quaternary structure by mechanical force. , 1977, Journal of molecular biology.

[10]  Y. Tu,et al.  Coordinated switching of bacterial flagellar motors: evidence for direct motor-motor coupling? , 2013, Physical review letters.

[11]  J. Sambrook,et al.  Molecular Cloning: A Laboratory Manual , 2001 .

[12]  Uri Alon,et al.  Response regulator output in bacterial chemotaxis , 1998, The EMBO journal.

[13]  Thierry Emonet,et al.  Hidden stochastic nature of a single bacterial motor. , 2006, Physical review letters.

[14]  C. V. Rao,et al.  FliZ Induces a Kinetic Switch in Flagellar Gene Expression , 2010, Journal of bacteriology.

[15]  Ido Golding,et al.  Chemotactic adaptation kinetics of individual Escherichia coli cells , 2012, Proceedings of the National Academy of Sciences.

[16]  Y. Tu,et al.  Logarithmic sensing in Escherichia coli bacterial chemotaxis. , 2009, Biophysical journal.

[17]  H. Berg,et al.  Chemotaxis in Escherichia coli analysed by Three-dimensional Tracking , 1972, Nature.

[18]  J. S. Parkinson,et al.  Isolation and behavior of Escherichia coli deletion mutants lacking chemotaxis functions , 1982, Journal of bacteriology.

[19]  H. Berg,et al.  Ultrasensitivity of an adaptive bacterial motor. , 2013, Journal of molecular biology.

[20]  G. Wadhams,et al.  Making sense of it all: bacterial chemotaxis , 2004, Nature Reviews Molecular Cell Biology.

[21]  Filipe Tostevin,et al.  Signaling noise enhances chemotactic drift of E. coli. , 2012, Physical review letters.

[22]  William S. Ryu,et al.  Real-Time Imaging of Fluorescent Flagellar Filaments , 2000, Journal of bacteriology.

[23]  Michael J. North,et al.  AgentCell: a digital single-cell assay for bacterial chemotaxis , 2005, Bioinform..

[24]  Matthew J Lang,et al.  Interlaced optical force-fluorescence measurements for single molecule biophysics. , 2006, Biophysical journal.

[25]  Pablo A. Iglesias,et al.  Optimal Noise Filtering in the Chemotactic Response of Escherichia coli , 2006, PLoS Comput. Biol..

[26]  C. V. Rao,et al.  FliZ Is a Posttranslational Activator of FlhD4C2-Dependent Flagellar Gene Expression , 2008, Journal of bacteriology.

[27]  Christopher V. Rao,et al.  High-resolution, long-term characterization of bacterial motility using optical tweezers , 2009, Nature Methods.

[28]  Christina Kluge,et al.  Data Reduction And Error Analysis For The Physical Sciences , 2016 .

[29]  J. Dobnikar,et al.  E. coli superdiffusion and chemotaxis-search strategy, precision, and motility. , 2009, Biophysical journal.

[30]  Nikita Vladimirov,et al.  Predicted Auxiliary Navigation Mechanism of Peritrichously Flagellated Chemotactic Bacteria , 2010, PLoS Comput. Biol..

[31]  C. Schmidt,et al.  Interference model for back-focal-plane displacement detection in optical tweezers. , 1998, Optics letters.

[32]  L. DeFelice.  E. coli in Motion , 2004, Biological and Medical Physics, Biomedical Engineering.

[33]  Lili Jiang,et al.  Quantitative Modeling of Escherichia coli Chemotactic Motion in Environments Varying in Space and Time , 2010, PLoS Comput. Biol..

[34]  J. S. Parkinson,et al.  A model of excitation and adaptation in bacterial chemotaxis. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[35]  Howard C. Berg,et al.  On Torque and Tumbling in Swimming Escherichia coli , 2006, Journal of bacteriology.

[36]  W. Wackernagel,et al.  Gene disruption in Escherichia coli: TcR and KmR cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. , 1995, Gene.

[37]  H. Bujard,et al.  Independent and tight regulation of transcriptional units in Escherichia coli via the LacR/O, the TetR/O and AraC/I1-I2 regulatory elements. , 1997, Nucleic acids research.

[38]  H. Berg,et al.  A modular gradient-sensing network for chemotaxis in Escherichia coli revealed by responses to time-varying stimuli , 2010, Molecular systems biology.

[39]  H. Berg,et al.  Coordination of flagella on filamentous cells of Escherichia coli , 1983, Journal of bacteriology.

[40]  N. Costantino,et al.  E. coli genome manipulation by P1 transduction. , 2007, Current protocols in molecular biology.

[41]  Howard C. Berg,et al.  Visualization of Flagella during Bacterial Swarming , 2010, Journal of bacteriology.

[42]  Hiroto Takahashi,et al.  Coordinated reversal of flagellar motors on a single Escherichia coli cell. , 2011, Biophysical journal.

[43]  H. Berg,et al.  Receptor sensitivity in bacterial chemotaxis , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[44]  J. Vilar,et al.  From molecular noise to behavioural variability in a single bacterium , 2004, Nature.

[45]  Howard C. Berg,et al.  Adaptation at the output of the chemotaxis signalling pathway , 2012, Nature.