IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-33816-6.html
   My bibliography  Save this article

Quorum-sensing control of matrix protein production drives fractal wrinkling and interfacial localization of Vibrio cholerae pellicles

Author

Listed:
  • Boyang Qin

    (Princeton University
    Princeton University)

  • Bonnie L. Bassler

    (Princeton University
    The Howard Hughes Medical Institute)

Abstract

Bacterial cells at fluid interfaces can self-assemble into collective communities with stunning macroscopic morphologies. Within these soft, living materials, called pellicles, constituent cells gain group-level survival advantages including increased antibiotic resistance. However, the regulatory and structural components that drive pellicle self-patterning are not well defined. Here, using Vibrio cholerae as our model system, we report that two sets of matrix proteins and a key quorum-sensing regulator jointly orchestrate the sequential mechanical instabilities underlying pellicle morphogenesis, culminating in fractal patterning. A pair of matrix proteins, RbmC and Bap1, maintain pellicle localization at the interface and prevent self-peeling. A single matrix protein, RbmA, drives a morphogenesis program marked by a cascade of ever finer wrinkles with fractal scaling in wavelength. Artificial expression of rbmA restores fractal wrinkling to a ΔrbmA mutant and enables precise tuning of fractal dimensions. The quorum-sensing regulatory small RNAs Qrr1-4 first activate matrix synthesis to launch pellicle primary wrinkling and ridge instabilities. Subsequently, via a distinct mechanism, Qrr1-4 suppress fractal wrinkling to promote fine modulation of pellicle morphology. Our results connect cell-cell signaling and architectural components to morphogenic patterning and suggest that manipulation of quorum-sensing regulators or synthetic control of rbmA expression could underpin strategies to engineer soft biomaterial morphologies on demand.

Suggested Citation

  • Boyang Qin & Bonnie L. Bassler, 2022. "Quorum-sensing control of matrix protein production drives fractal wrinkling and interfacial localization of Vibrio cholerae pellicles," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-33816-6
    DOI: 10.1038/s41467-022-33816-6
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-33816-6
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-33816-6?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. Geoffrey B. West & James H. Brown & Brian J. Enquist, 1999. "The Fourth Dimension of Life: Fractal Geometry and Allometric Scaling of Organisms," Working Papers 99-07-047, Santa Fe Institute.
    2. Thierry Savin & Natasza A. Kurpios & Amy E. Shyer & Patricia Florescu & Haiyi Liang & L. Mahadevan & Clifford J. Tabin, 2011. "On the growth and form of the gut," Nature, Nature, vol. 476(7358), pages 57-62, August.
    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. Scott G Ortman & José Lobo & Michael E Smith, 2020. "Cities: Complexity, theory and history," PLOS ONE, Public Library of Science, vol. 15(12), pages 1-24, December.
    2. He, Ji-Huan & Liu, Jun-Fang, 2009. "Allometric scaling laws in biology and physics," Chaos, Solitons & Fractals, Elsevier, vol. 41(4), pages 1836-1838.
    3. Brolly, Matthew & Woodhouse, Iain H., 2012. "A “Matchstick Model” of microwave backscatter from a forest," Ecological Modelling, Elsevier, vol. 237, pages 74-87.
    4. Dalgaard, Carl-Johan & Strulik, Holger, 2011. "Energy distribution and economic growth," Resource and Energy Economics, Elsevier, vol. 33(4), pages 782-797.
    5. Husmann, Kai & Möhring, Bernhard, 2017. "Modelling the economically viable wood in the crown of European beech trees," Forest Policy and Economics, Elsevier, vol. 78(C), pages 67-77.
    6. He, Ji-Huan, 2006. "An allometric scaling law between gray matter and white matter of cerebral cortex," Chaos, Solitons & Fractals, Elsevier, vol. 27(4), pages 864-867.
    7. Tao, Yong & Lin, Li & Wang, Hanjie & Hou, Chen, 2023. "Superlinear growth and the fossil fuel energy sustainability dilemma: Evidence from six continents," Structural Change and Economic Dynamics, Elsevier, vol. 66(C), pages 39-51.
    8. Patrick D McMullen & Erin Z Aprison & Peter B Winter & Luis A N Amaral & Richard I Morimoto & Ilya Ruvinsky, 2012. "Macro-level Modeling of the Response of C. elegans Reproduction to Chronic Heat Stress," PLOS Computational Biology, Public Library of Science, vol. 8(1), pages 1-12, January.
    9. Jiao Li & Yongsheng Qian & Junwei Zeng & Fan Yin & Leipeng Zhu & Xiaoping Guang, 2020. "Research on the Influence of a High-Speed Railway on the Spatial Structure of the Western Urban Agglomeration Based on Fractal Theory—Taking the Chengdu–Chongqing Urban Agglomeration as an Example," Sustainability, MDPI, vol. 12(18), pages 1-13, September.
    10. Chen, Yanguang, 2017. "Multi-scaling allometric analysis for urban and regional development," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 465(C), pages 673-689.
    11. Torres-Rojo, Juan Manuel & Francisco-Cruz, Carlos Alberto & Islas-Aguirre, Juan Francisco & Ramírez-Fuentes, Grodecz Alfredo & Pérez-Sosa, Leonardo, 2020. "A scale invariant model for the expansion of agricultural land and government spending on the agricultural sector," Land Use Policy, Elsevier, vol. 92(C).
    12. Peters, Ronny & Olagoke, Adewole & Berger, Uta, 2018. "A new mechanistic theory of self-thinning: Adaptive behaviour of plants explains the shape and slope of self-thinning trajectories," Ecological Modelling, Elsevier, vol. 390(C), pages 1-9.
    13. GANIO-MEGO, Joe, 2022. "Estimating the human equivalent weight by applying the quarter-power law of allometry to humanity," OSF Preprints 7eq6x, Center for Open Science.
    14. Song, Dong-Ming & Jiang, Zhi-Qiang & Zhou, Wei-Xing, 2009. "Statistical properties of world investment networks," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 388(12), pages 2450-2460.
    15. Tyson L Swetnam & Christopher D O’Connor & Ann M Lynch, 2016. "Tree Morphologic Plasticity Explains Deviation from Metabolic Scaling Theory in Semi-Arid Conifer Forests, Southwestern USA," PLOS ONE, Public Library of Science, vol. 11(7), pages 1-16, July.
    16. GANIO-MEGO, Joe, 2022. "Long term world human population, lifespan and GDP growth model based on the in-caput-evolution theory and its impact on the carrying capacity," OSF Preprints dm3jn, Center for Open Science.
    17. Christopher Watts & Nigel Gilbert, 2014. "Simulating Innovation," Books, Edward Elgar Publishing, number 13981, December.
    18. Liu, Chuang & Zhou, Wei-Xing & Yuan, Wei-Kang, 2010. "Statistical properties of visibility graph of energy dissipation rates in three-dimensional fully developed turbulence," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 389(13), pages 2675-2681.
    19. Calabrese, Armando & Capece, Guendalina & Costa, Roberta & Di Pillo, Francesca & Giuffrida, Stefania, 2018. "A ‘power law’ based method to reduce size-related bias in indicators of knowledge performance: An application to university research assessment," Journal of Informetrics, Elsevier, vol. 12(4), pages 1263-1281.
    20. Wilfred M. Wollheim & Tamara K. Harms & Andrew L. Robison & Lauren E. Koenig & Ashley M. Helton & Chao Song & William B. Bowden & Jacques C. Finlay, 2022. "Superlinear scaling of riverine biogeochemical function with watershed size," Nature Communications, Nature, vol. 13(1), pages 1-9, 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:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-33816-6. 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: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    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.