Proliferation of Yeast in Complex Environments

Abstract

Despite the extensive role yeast plays across disciplines, our understanding of its growth and pathogenesis has been constrained to studies of yeast cultivated in bulk liquid media, typically on two-dimensional plates, or chemostat cultures. Such settings do not reflect the complex three-dimensional environments yeast inhabit in nature. The natural habitat for yeast, such as eukaryotic cells, tissues, soil, and biological gels, have porous microstructure and complex mechanical properties. Through direct imaging of yeast colonies in transparent three-dimensional viscoplastic microgels with tunable mechanical properties, we study the proliferation of yeast grown under spatially nonuniform oxygen availability, elucidate the adaptive response of yeast to spatial confinement and nutrient limitations, and explore their invasive growth within a porous medium. We show that due to spatially nonuniform oxygen availability, respiring yeast only grows on the surface where the oxygen concentration is sufficient. However, fermenting yeast exhibits a less steep spatial growth gradient as a result of self-generated oxygen gradient. We found that dense yeast colonies can leverage on bubble entrainment to break out of the nutrient-depleted core. Finally, we observed that a mutant yeast strain switches its vegetative budding pattern to an invasive one when grown in the hydrogels matrix, hinting at a connection between the mechanical properties of the environment and yeast’s budding behavior. This study sheds light on the intricate coupling between a yeast colony and its surroundings, and the ways in which mechanical properties of the environment can impact the proliferation of yeast. It underscores the importance of studying the biophysics of yeast in realistic complex environments and lays the groundwork for future investigations.