IDEAS home Printed from https://ideas.repec.org/a/plo/pcbi00/1002361.html
   My bibliography  Save this article

Prediction by Promoter Logic in Bacterial Quorum Sensing

Author

Listed:
  • Navneet Rai
  • Rajat Anand
  • Krishna Ramkumar
  • Varun Sreenivasan
  • Sugat Dabholkar
  • K V Venkatesh
  • Mukund Thattai

Abstract

Quorum-sensing systems mediate chemical communication between bacterial cells, coordinating cell-density-dependent processes like biofilm formation and virulence-factor expression. In the proteobacterial LuxI/LuxR quorum sensing paradigm, a signaling molecule generated by an enzyme (LuxI) diffuses between cells and allosterically stimulates a transcriptional regulator (LuxR) to activate its cognate promoter (pR). By expressing either LuxI or LuxR in positive feedback from pR, these versatile systems can generate smooth (monostable) or abrupt (bistable) density-dependent responses to suit the ecological context. Here we combine theory and experiment to demonstrate that the promoter logic of pR – its measured activity as a function of LuxI and LuxR levels – contains all the biochemical information required to quantitatively predict the responses of such feedback loops. The interplay of promoter logic with feedback topology underlies the versatility of the LuxI/LuxR paradigm: LuxR and LuxI positive-feedback systems show dramatically different responses, while a dual positive/negative-feedback system displays synchronized oscillations. These results highlight the dual utility of promoter logic: to probe microscopic parameters and predict macroscopic phenotype. Author Summary: Bacterial cells constantly communicate with one another by exchanging chemical signals, which constitute a rich source of information about the proximity of friends or foes in the environment. These signals can be used to coordinate the actions of cells across a population. For example, pathogenic bacteria infecting a host can remain quiescent, only becoming virulent once they attain a sufficient cell density. Such coordination, regulated by so-called quorum-sensing systems, works on the following principle: every cell in the population secretes a specific chemical signal; the more cells there are, the more signal is generated; when individual cells sense that the signal has crossed some threshold, they launch a response. The nature of the response depends on the detailed molecular wiring of the secretion and sensing system, which can vary from species to species. It is often impossible to determine all these molecular details for any given system. Borrowing ideas from control theory, we show that this internal wiring can be largely ignored, and these systems can be considered as ‘black boxes’. Our experiments demonstrate that the measured input-output logic of the black box, which we term ‘promoter logic’, is sufficient to predict the diverse responses of different quorum-sensing systems.

Suggested Citation

  • Navneet Rai & Rajat Anand & Krishna Ramkumar & Varun Sreenivasan & Sugat Dabholkar & K V Venkatesh & Mukund Thattai, 2012. "Prediction by Promoter Logic in Bacterial Quorum Sensing," PLOS Computational Biology, Public Library of Science, vol. 8(1), pages 1-14, January.
  • Handle: RePEc:plo:pcbi00:1002361
    DOI: 10.1371/journal.pcbi.1002361
    as

    Download full text from publisher

    File URL: https://journals.plos.org/ploscompbiol/article?id=10.1371/journal.pcbi.1002361
    Download Restriction: no

    File URL: https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1002361&type=printable
    Download Restriction: no

    File URL: https://libkey.io/10.1371/journal.pcbi.1002361?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. Alvin Tamsir & Jeffrey J. Tabor & Christopher A. Voigt, 2011. "Robust multicellular computing using genetically encoded NOR gates and chemical ‘wires’," Nature, Nature, vol. 469(7329), pages 212-215, January.
    2. Nicholas J. Guido & Xiao Wang & David Adalsteinsson & David McMillen & Jeff Hasty & Charles R. Cantor & Timothy C. Elston & J. J. Collins, 2006. "A bottom-up approach to gene regulation," Nature, Nature, vol. 439(7078), pages 856-860, February.
    3. Ertugrul M. Ozbudak & Mukund Thattai & Han N. Lim & Boris I. Shraiman & Alexander van Oudenaarden, 2004. "Multistability in the lactose utilization network of Escherichia coli," Nature, Nature, vol. 427(6976), pages 737-740, February.
    4. Tal Danino & Octavio Mondragón-Palomino & Lev Tsimring & Jeff Hasty, 2010. "A synchronized quorum of genetic clocks," Nature, Nature, vol. 463(7279), pages 326-330, January.
    Full references (including those not matched with items on IDEAS)

    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. 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.
    2. Alice Boo & Tyler Toth & Qiguo Yu & Alexander Pfotenhauer & Brandon D. Fields & Scott C. Lenaghan & C. Neal Stewart & Christopher A. Voigt, 2024. "Synthetic microbe-to-plant communication channels," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    3. 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.
    4. Masa Tsuchiya & Vincent Piras & Alessandro Giuliani & Masaru Tomita & Kumar Selvarajoo, 2010. "Collective Dynamics of Specific Gene Ensembles Crucial for Neutrophil Differentiation: The Existence of Genome Vehicles Revealed," PLOS ONE, Public Library of Science, vol. 5(8), pages 1-10, August.
    5. Lai, Qiang & Norouzi, Benyamin & Liu, Feng, 2018. "Dynamic analysis, circuit realization, control design and image encryption application of an extended Lü system with coexisting attractors," Chaos, Solitons & Fractals, Elsevier, vol. 114(C), pages 230-245.
    6. 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.
    7. Paul Miller & Anatol M Zhabotinsky & John E Lisman & Xiao-Jing Wang, 2005. "The Stability of a Stochastic CaMKII Switch: Dependence on the Number of Enzyme Molecules and Protein Turnover," PLOS Biology, Public Library of Science, vol. 3(4), pages 1-1, March.
    8. Matthieu Wyart & David Botstein & Ned S Wingreen, 2010. "Evaluating Gene Expression Dynamics Using Pairwise RNA FISH Data," PLOS Computational Biology, Public Library of Science, vol. 6(11), pages 1-14, November.
    9. Weiyue Ji & Handuo Shi & Haoqian Zhang & Rui Sun & Jingyi Xi & Dingqiao Wen & Jingchen Feng & Yiwei Chen & Xiao Qin & Yanrong Ma & Wenhan Luo & Linna Deng & Hanchi Lin & Ruofan Yu & Qi Ouyang, 2013. "A Formalized Design Process for Bacterial Consortia That Perform Logic Computing," PLOS ONE, Public Library of Science, vol. 8(2), pages 1-9, February.
    10. Onelia Gagliano & Camilla Luni & Yan Li & Silvia Angiolillo & Wei Qin & Francesco Panariello & Davide Cacchiarelli & Joseph S. Takahashi & Nicola Elvassore, 2021. "Synchronization between peripheral circadian clock and feeding-fasting cycles in microfluidic device sustains oscillatory pattern of transcriptome," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    11. Georg Fritz & Judith A Megerle & Sonja A Westermayer & Delia Brick & Ralf Heermann & Kirsten Jung & Joachim O Rädler & Ulrich Gerland, 2014. "Single Cell Kinetics of Phenotypic Switching in the Arabinose Utilization System of E. coli," PLOS ONE, Public Library of Science, vol. 9(2), pages 1-12, February.
    12. Najme Khorasani & Mehdi Sadeghi & Abbas Nowzari-Dalini, 2020. "A computational model of stem cell molecular mechanism to maintain tissue homeostasis," PLOS ONE, Public Library of Science, vol. 15(7), pages 1-25, July.
    13. Jan Hasenauer & Christine Hasenauer & Tim Hucho & Fabian J Theis, 2014. "ODE Constrained Mixture Modelling: A Method for Unraveling Subpopulation Structures and Dynamics," PLOS Computational Biology, Public Library of Science, vol. 10(7), pages 1-17, July.
    14. Tai-Yin Chiu & Hui-Ju K Chiang & Ruei-Yang Huang & Jie-Hong R Jiang & François Fages, 2015. "Synthesizing Configurable Biochemical Implementation of Linear Systems from Their Transfer Function Specifications," PLOS ONE, Public Library of Science, vol. 10(9), pages 1-27, September.
    15. Nagarajan, Radhakrishnan, 2007. "Delay estimation in a two-node acyclic network," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 376(C), pages 725-737.
    16. 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.
    17. Keun-Young Kim & Jin Wang, 2007. "Potential Energy Landscape and Robustness of a Gene Regulatory Network: Toggle Switch," PLOS Computational Biology, Public Library of Science, vol. 3(3), pages 1-13, March.
    18. Song, Yi & Xu, Wei & Wei, Wei & Niu, Lizhi, 2023. "Dynamical transition of phenotypic states in breast cancer system with Lévy noise," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 627(C).
    19. Lukas Aufinger & Johann Brenner & Friedrich C. Simmel, 2022. "Complex dynamics in a synchronized cell-free genetic clock," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    20. Alex J. H. Fedorec & Neythen J. Treloar & Ke Yan Wen & Linda Dekker & Qing Hsuan Ong & Gabija Jurkeviciute & Enbo Lyu & Jack W. Rutter & Kathleen J. Y. Zhang & Luca Rosa & Alexey Zaikin & Chris P. Bar, 2024. "Emergent digital bio-computation through spatial diffusion and engineered bacteria," Nature Communications, Nature, vol. 15(1), pages 1-11, 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:pcbi00:1002361. 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.