Hierarchical transitions and fractal wrinkling drive bacterial pellicle morphogenesis.

Hierarchical transitions and fractal wrinkling drive bacterial pellicle morphogenesis.
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DOI:
10.1073/pnas.2023504118
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发表时间:
2021-05-18
影响因子:
11.1
通讯作者:
Bassler BL
Bassler BL
中科院分区:
综合性期刊1区
文献类型:
--
作者:
Qin B;Fei C;Wang B;Stone HA;Wingreen NS;Bassler BL

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Multicellular bacterial communities called biofilms and pellicles significantly influence medical infections and industrial biofouling. Biofilms and pellicles often act as reservoirs of toxigenic bacteria. Here, we report a fractal wrinkling morphogenesis program that underlies pellicle formation in the model biofilm former and global pathogen, Vibrio cholerae. Pellicle morphogenesis is marked by the emergence of a cascade of self-similar structures with fractal-like scaling in wavelength, which increases surface area and presumably enhances nutrient transport and signaling among community members. This morphogenesis program can be altered by varying the spatial heterogeneity of the community. Thus, bacterial pellicles could provide tractable model systems to understand overarching principles driving morphogenesis and for engineering of functional soft biomaterials. Bacterial cells can self-organize into structured communities at fluid–fluid interfaces. These soft, living materials composed of cells and extracellular matrix are called pellicles. Cells residing in pellicles garner group-level survival advantages such as increased antibiotic resistance. The dynamics of pellicle formation and, more generally, how complex morphologies arise from active biomaterials confined at interfaces are not well understood. Here, using Vibrio cholerae as our model organism, a custom-built adaptive stereo microscope, fluorescence imaging, mechanical theory, and simulations, we report a fractal wrinkling morphogenesis program that differs radically from the well-known coalescence of wrinkles into folds that occurs in passive thin films at fluid–fluid interfaces. Four stages occur: growth of founding colonies, onset of primary wrinkles, development of secondary curved ridge instabilities, and finally the emergence of a cascade of finer structures with fractal-like scaling in wavelength. The time evolution of pellicle formation depends on the initial heterogeneity of the film microstructure. Changing the starting bacterial seeding density produces three variations in the sequence of morphogenic stages, which we term the bypass, crystalline, and incomplete modes. Despite these global architectural transitions, individual microcolonies remain spatially segregated, and thus, the community maintains spatial and genetic heterogeneity. Our results suggest that the memory of the original microstructure is critical in setting the morphogenic dynamics of a pellicle as an active biomaterial.
DOI: 10.1073/pnas.50.3.576
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