Hierarchical transitions and fractal wrinkling drive bacterial pellicle morphogenesis.

TitleHierarchical transitions and fractal wrinkling drive bacterial pellicle morphogenesis.
Publication TypeJournal Article
Year of Publication2021
AuthorsQin, B, Fei, C, Wang, B, Stone, HA, Wingreen, NS, Bassler, BL
JournalProc Natl Acad Sci U S A
Volume118
Issue20
Date Published2021 May 18
ISSN1091-6490
Abstract

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 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.

DOI10.1073/pnas.2023504118
Alternate JournalProc Natl Acad Sci U S A
PubMed ID33972433
PubMed Central IDPMC8157956