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1. Hierarchical Transitions and Fractal Wrinkling Drive Bacterial Pellicle Morphogenesis

   Qin, B.; Fei, C.; Wang, B.; Stone, H.A.; Wingreen, N.S.; Bassler, B.L. (April 2021, Proceedings of the National Academy of Sciences of the United States of America)

   null (Ed.)

   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. 

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

   https://doi.org/10.1038/s41467-022-33816-6  

   Qin, Boyang; Bassler, Bonnie L. (October 2022, Nature Communications)

   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, usingVibrio choleraeas 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 ofrbmArestores fractal wrinkling to a ΔrbmAmutant 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 ofrbmAexpression could underpin strategies to engineer soft biomaterial morphologies on demand. 

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3. Role of Staphylococcus aureus’s Buoyant Density in the Development of Biofilm Associated Antibiotic Susceptibility

   https://doi.org/10.3390/microorganisms12040759  

   Kispert, Sarah; Liguori, Madison; Velikaneye, Cody; Qiu, Chong; Wang, Shue; Zhang, Nan; Gu, Huan (April 2024, Microorganisms)

   Biofilms are clusters of microorganisms that form at various interfaces, including those between air and liquid or liquid and solid. Due to their roles in enhancing wastewater treatment processes, and their unfortunate propensity to cause persistent human infections through lowering antibiotic susceptibility, understanding and managing bacterial biofilms is of paramount importance. A pivotal stage in biofilm development is the initial bacterial attachment to these interfaces. However, the determinants of bacterial cell choice in colonizing an interface first and heterogeneity in bacterial adhesion remain elusive. Our research has unveiled variations in the buoyant density of free-swimming Staphylococcus aureus cells, irrespective of their growth phase. Cells with a low cell buoyant density, characterized by fewer cell contents, exhibited lower susceptibility to antibiotic treatments (100 μg/mL vancomycin) and favored biofilm formation at air–liquid interfaces. In contrast, cells with higher cell buoyant density, which have richer cell contents, were more vulnerable to antibiotics and predominantly formed biofilms on liquid–solid interfaces when contained upright. Cells with low cell buoyant density were not able to revert to a more antibiotic sensitive and high cell buoyant density phenotype. In essence, S. aureus cells with higher cell buoyant density may be more inclined to adhere to upright substrates. 

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4. Janus particle amphiphilicity and capillary interactions at a fluid interface

   https://doi.org/10.1002/aic.18241  

   Correia, Elton_L; Razavi, Sepideh (September 2023, AIChE Journal)

   Abstract Studying the behavior of anisotropic particles at fluid interfaces is a rapidly expanding field, as understanding how the introduced anisotropy affects the resulting properties is essential in the engineering of interfacial systems. Surface anisotropic particles, also known as Janus particles (JPs), offer new possibilities for novel applications due to their amphiphilicity and stronger binding to fluid interfaces compared to homogeneous particles. Introducing surface anisotropy creates complexity as the orientation of interfacially bound particles affects interparticle interactions, a contributing factor to the microstructure formation. In this work, we have investigated the microstructure of JP monolayers formed at the air–water interface using particles with different degrees of amphiphilicity and examined the response of the networks to applied compressions. Our findings demonstrate that JPs amphiphilicity is a crucial factor governing their orientation at the interface, which in turn dictates the complexity of the capillary interactions present and the mechanical properties of the ensuing networks. 

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5. Spatial–temporal order–disorder transition in angiogenic NOTCH signaling controls cell fate specification

   https://doi.org/10.7554/eLife.89262  

   Kang, Tae-Yun; Bocci, Federico; Nie, Qing; Onuchic, José N; Levchenko, Andre (February 2024, eLife)

   Angiogenesis is a morphogenic process resulting in the formation of new blood vessels from pre-existing ones, usually in hypoxic micro-environments. The initial steps of angiogenesis depend on robust differentiation of oligopotent endothelial cells into the Tip and Stalk phenotypic cell fates, controlled by NOTCH-dependent cell–cell communication. The dynamics of spatial patterning of this cell fate specification are only partially understood. Here, by combining a controlled experimental angiogenesis model with mathematical and computational analyses, we find that the regular spatial Tip–Stalk cell patterning can undergo an order–disorder transition at a relatively high input level of a pro-angiogenic factor VEGF. The resulting differentiation is robust but temporally unstable for most cells, with only a subset of presumptive Tip cells leading sprout extensions. We further find that sprouts form in a manner maximizing their mutual distance, consistent with a Turing-like model that may depend on local enrichment and depletion of fibronectin. Together, our data suggest that NOTCH signaling mediates a robust way of cell differentiation enabling but not instructing subsequent steps in angiogenic morphogenesis, which may require additional cues and self-organization mechanisms. This analysis can assist in further understanding of cell plasticity underlying angiogenesis and other complex morphogenic processes. 

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