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

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  • 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
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    1. 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.
    2. 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.
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