IDEAS home Printed from https://ideas.repec.org/a/plo/pcbi00/1002172.html
   My bibliography  Save this article

LsrR Quorum Sensing “Switch” Is Revealed by a Bottom-Up Approach

Author

Listed:
  • Sara Hooshangi
  • William E Bentley

Abstract

Quorum sensing (QS) enables bacterial multicellularity and selective advantage for communicating populations. While genetic “switching” phenomena are a common feature, their mechanistic underpinnings have remained elusive. The interplay between circuit components and their regulation are intertwined and embedded. Observable phenotypes are complex and context dependent. We employed a combination of experimental work and mathematical models to decipher network connectivity and signal transduction in the autoinducer-2 (AI-2) quorum sensing system of E. coli. Negative and positive feedback mechanisms were examined by separating the network architecture into sub-networks. A new unreported negative feedback interaction was hypothesized and tested via a simple mathematical model. Also, the importance of the LsrR regulator and its determinant role in the E. coli QS “switch”, normally masked by interfering regulatory loops, were revealed. Our simple model allowed mechanistic understanding of the interplay among regulatory sub-structures and their contributions to the overall native functioning network. This “bottom up” approach in understanding gene regulation will serve to unravel complex QS network architectures and lead to the directed coordination of emergent behaviors. Author Summary: Quorum sensing is a mechanism by which bacterial cells communicate within a population. One particular form of communication in E. coli is through a universal signaling molecule known as autoinducer 2. Although the importance of this form of cell-cell interaction has been recognized in the formation of biofilms and virulent infections, the mechanisms by which this form of communication is regulated is still not well understood. In this paper, we presented a method of unraveling these mechanisms by using a combination of experimental work and mathematical models. We took apart the network architecture and isolated the different components. The examination of these isolated sub-networks provided us with a better understanding of the underlying mechanisms that control and regulate bacterial quorum sensing. We were also able to predict new network interactions with the help of our mathematical models. This bottom up approach, combined with our modeling efforts, proved effective in unraveling the mechanisms of quorum sensing in E. coli.

Suggested Citation

  • Sara Hooshangi & William E Bentley, 2011. "LsrR Quorum Sensing “Switch” Is Revealed by a Bottom-Up Approach," PLOS Computational Biology, Public Library of Science, vol. 7(9), pages 1-11, September.
  • Handle: RePEc:plo:pcbi00:1002172
    DOI: 10.1371/journal.pcbi.1002172
    as

    Download full text from publisher

    File URL: https://journals.plos.org/ploscompbiol/article?id=10.1371/journal.pcbi.1002172
    Download Restriction: no

    File URL: https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1002172&type=printable
    Download Restriction: no

    File URL: https://libkey.io/10.1371/journal.pcbi.1002172?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Richard C. Yu & C. Gustavo Pesce & Alejandro Colman-Lerner & Larry Lok & David Pincus & Eduard Serra & Mark Holl & Kirsten Benjamin & Andrew Gordon & Roger Brent, 2008. "Negative feedback that improves information transmission in yeast signalling," Nature, Nature, vol. 456(7223), pages 755-761, December.
    2. Attila Becskei & Luis Serrano, 2000. "Engineering stability in gene networks by autoregulation," Nature, Nature, vol. 405(6786), pages 590-593, June.
    3. Marcel Tigges & Tatiana T. Marquez-Lago & Jörg Stelling & Martin Fussenegger, 2009. "A tunable synthetic mammalian oscillator," Nature, Nature, vol. 457(7227), pages 309-312, January.
    4. Jesse Stricker & Scott Cookson & Matthew R. Bennett & William H. Mather & Lev S. Tsimring & Jeff Hasty, 2008. "A fast, robust and tunable synthetic gene oscillator," Nature, Nature, vol. 456(7221), pages 516-519, November.
    5. Timothy S. Gardner & Charles R. Cantor & James J. Collins, 2000. "Construction of a genetic toggle switch in Escherichia coli," Nature, Nature, vol. 403(6767), pages 339-342, January.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. David Scheidweiler & Ankur Deep Bordoloi & Wenqiao Jiao & Vladimir Sentchilo & Monica Bollani & Audam Chhun & Philipp Engel & Pietro de Anna, 2024. "Spatial structure, chemotaxis and quorum sensing shape bacterial biomass accumulation in complex porous media," Nature Communications, Nature, vol. 15(1), pages 1-12, December.

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Zhou, Peipei & Cai, Shuiming & Liu, Zengrong & Chen, Luonan & Wang, Ruiqi, 2013. "Coupling switches and oscillators as a means to shape cellular signals in biomolecular systems," Chaos, Solitons & Fractals, Elsevier, vol. 50(C), pages 115-126.
    2. Lucia Marucci & David A W Barton & Irene Cantone & Maria Aurelia Ricci & Maria Pia Cosma & Stefania Santini & Diego di Bernardo & Mario di Bernardo, 2009. "How to Turn a Genetic Circuit into a Synthetic Tunable Oscillator, or a Bistable Switch," PLOS ONE, Public Library of Science, vol. 4(12), pages 1-10, December.
    3. Miles Miller & Marc Hafner & Eduardo Sontag & Noah Davidsohn & Sairam Subramanian & Priscilla E M Purnick & Douglas Lauffenburger & Ron Weiss, 2012. "Modular Design of Artificial Tissue Homeostasis: Robust Control through Synthetic Cellular Heterogeneity," PLOS Computational Biology, Public Library of Science, vol. 8(7), pages 1-18, July.
    4. Avraham E Mayo & Yaakov Setty & Seagull Shavit & Alon Zaslaver & Uri Alon, 2006. "Plasticity of the cis-Regulatory Input Function of a Gene," PLOS Biology, Public Library of Science, vol. 4(4), pages 1-1, March.
    5. Astakhov, Sergey & Astakhov, Oleg & Fadeeva, Natalia & Astakhov, Vladimir, 2021. "Multistability, quasiperiodicity and chaos in a self-oscillating ring dynamical system with three degrees of freedom based on the van der Pol generator," Chaos, Solitons & Fractals, Elsevier, vol. 148(C).
    6. Tobias May & Lee Eccleston & Sabrina Herrmann & Hansjörg Hauser & Jorge Goncalves & Dagmar Wirth, 2008. "Bimodal and Hysteretic Expression in Mammalian Cells from a Synthetic Gene Circuit," PLOS ONE, Public Library of Science, vol. 3(6), pages 1-7, June.
    7. Evgeni V Nikolaev & Eduardo D Sontag, 2016. "Quorum-Sensing Synchronization of Synthetic Toggle Switches: A Design Based on Monotone Dynamical Systems Theory," PLOS Computational Biology, Public Library of Science, vol. 12(4), pages 1-33, April.
    8. Singh, Vijai & Chaudhary, Dharmendra Kumar & Mani, Indra & Dhar, Pawan Kumar, 2016. "Recent advances and challenges of the use of cyanobacteria towards the production of biofuels," Renewable and Sustainable Energy Reviews, Elsevier, vol. 60(C), pages 1-10.
    9. Luca Cardelli & Rosa D Hernansaiz-Ballesteros & Neil Dalchau & Attila Csikász-Nagy, 2017. "Efficient Switches in Biology and Computer Science," PLOS Computational Biology, Public Library of Science, vol. 13(1), pages 1-16, January.
    10. Samanthe M Lyons & Wenlong Xu & June Medford & Ashok Prasad, 2014. "Loads Bias Genetic and Signaling Switches in Synthetic and Natural Systems," PLOS Computational Biology, Public Library of Science, vol. 10(3), pages 1-16, March.
    11. Alan Veliz-Cuba & Andrew J Hirning & Adam A Atanas & Faiza Hussain & Flavia Vancia & Krešimir Josić & Matthew R Bennett, 2015. "Sources of Variability in a Synthetic Gene Oscillator," PLOS Computational Biology, Public Library of Science, vol. 11(12), pages 1-23, December.
    12. Betz, Ulrich A.K. & Arora, Loukik & Assal, Reem A. & Azevedo, Hatylas & Baldwin, Jeremy & Becker, Michael S. & Bostock, Stefan & Cheng, Vinton & Egle, Tobias & Ferrari, Nicola & Schneider-Futschik, El, 2023. "Game changers in science and technology - now and beyond," Technological Forecasting and Social Change, Elsevier, vol. 193(C).
    13. Stefano Ciliberti & Olivier C Martin & Andreas Wagner, 2007. "Robustness Can Evolve Gradually in Complex Regulatory Gene Networks with Varying Topology," PLOS Computational Biology, Public Library of Science, vol. 3(2), pages 1-10, February.
    14. Graham Rockwell & Nicholas J Guido & George M Church, 2013. "Redirector: Designing Cell Factories by Reconstructing the Metabolic Objective," PLOS Computational Biology, Public Library of Science, vol. 9(1), pages 1-15, January.
    15. Jiegen Wu & Baoqiang Chen & Yadi Liu & Liang Ma & Wen Huang & Yihan Lin, 2022. "Modulating gene regulation function by chemically controlled transcription factor clustering," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    16. Wu, Juan & Xu, Yong & Ma, Shaojuan, 2019. "Realizing the transformation of logic gates in a genetic toggle system under Lévy noise," Chaos, Solitons & Fractals, Elsevier, vol. 119(C), pages 171-179.
    17. Luna Rizik & Loai Danial & Mouna Habib & Ron Weiss & Ramez Daniel, 2022. "Synthetic neuromorphic computing in living cells," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    18. Shunsuke Kawasaki & Hiroki Ono & Moe Hirosawa & Takeru Kuwabara & Shunsuke Sumi & Suji Lee & Knut Woltjen & Hirohide Saito, 2023. "Programmable mammalian translational modulators by CRISPR-associated proteins," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    19. Cencetti, Giulia & Battiston, Federico & Carletti, Timoteo & Fanelli, Duccio, 2020. "Generalized patterns from local and non local reactions," Chaos, Solitons & Fractals, Elsevier, vol. 134(C).
    20. Tomas Tokar & Jozef Ulicny, 2013. "The Mathematical Model of the Bcl-2 Family Mediated MOMP Regulation Can Perform a Non-Trivial Pattern Recognition," PLOS ONE, Public Library of Science, vol. 8(12), pages 1-8, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:plo:pcbi00:1002172. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: ploscompbiol (email available below). General contact details of provider: https://journals.plos.org/ploscompbiol/ .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.