Two-Dimensionality of Yeast Colony Expansion Accompanied by Pattern Formation

Yeasts can form multicellular patterns as they expand on agar plates, a phenotype that requires a functional copy of the FLO11 gene. Although the biochemical and molecular requirements for such patterns have been examined, the mechanisms underlying their formation are not entirely clear. Here we develop quantitative methods to accurately characterize the size, shape, and surface patterns of yeast colonies for various combinations of agar and sugar concentrations. We combine these measurements with mathematical and physical models and find that FLO11 gene constrains cells to grow near the agar surface, causing the formation of larger and more irregular colonies that undergo hierarchical wrinkling. Head-to-head competition assays on agar plates indicate that two-dimensional constraint on the expansion of FLO11 wild type (FLO11) cells confers a fitness advantage over FLO11 knockout (flo11Δ) cells on the agar surface.Author Summary: Microbial biofilms are commonly found in nature and are highly relevant to public health. Biofilms can impose high risks to drinking water distribution by stable adherence to the interior of water pipes, and to food industry by contamination of food processing systems. Biofilm adherence to indwelling medical devices causes high rates of clinical infections that are difficult to eliminate as biofilm microbes resist treatment with antibiotics and biocides. These microbial abilities are related to the spatial composition and overall morphology of the biofilm. While the mechanisms underlying biofilm structure and morphology have been examined for bacteria, much less is known about eukaryotic biofilms. Here we find that the size, shape and patterning of budding yeast colonies can arise from constraining colony expansion to the surface of agar plates. Through computational analysis and mathematical modeling, we find that rapid colony expansion, colony shape irregularity and hierarchical wrinkling of the yeast colony surface can result from two-dimensionality of expansion imposed by the adhesin FLO11. Finally, we find that two-dimensional expansion conveys competitive advantage during head-to-head competition with the mutant cells lacking FLO11.