Environmental and Genetic Determinants of Colony Morphology in Yeast

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Abstract
Nutrient stresses trigger a variety of developmental switches in the budding yeast Saccharomyces cerevisiae. One of the least understood of such responses is the development of complex colony morphology, characterized by intricate, organized, and strain-specific patterns of colony growth and architecture. The genetic bases of this phenotype and the key environmental signals involved in its induction have heretofore remained poorly understood. By surveying multiple strain backgrounds and a large number of growth conditions, we show that limitation for fermentable carbon sources coupled with a rich nitrogen source is the primary trigger for the colony morphology response in budding yeast. Using knockout mutants and transposon-mediated mutagenesis, we demonstrate that two key signaling networks regulating this response are the filamentous growth MAP kinase cascade and the Ras-cAMP-PKA pathway. We further show synergistic epistasis between Rim15, a kinase involved in integration of nutrient signals, and other genes in these pathways. Ploidy, mating-type, and genotype-by-environment interactions also appear to play a role in the controlling colony morphology. Our study highlights the high degree of network reuse in this model eukaryote; yeast use the same core signaling pathways in multiple contexts to integrate information about environmental and physiological states and generate diverse developmental outputs. Baker's yeast forms smooth round colonies when grown in favorable conditions. When starved for one or more nutrients, yeast can alter its growth pattern to produce complex structures consisting of numerous interacting cells. One mode of growth, the colony morphology response, produces visually striking, lacy colony architectures. We describe both conditions that induce this morphology and also genes and pathways that are required for the response. We demonstrate that low levels of carbon combined with abundant nitrogen trigger complex colony formation. Using a candidate gene approach coupled with genome-wide mutagenesis, we identified genes involved in the production of complex colony morphology. Many of these genes are components of either a MAP kinase cascade or the Ras-cAMP-PKA pathway, two well-studied signaling pathways that are conserved across eukaryotic organisms. Yeast use these pathways to mediate cellular responses to changes in their environment. We observe shared characteristics between complex colonies and biofilms, which are organized communities of microorganisms with relevance to human health and human infrastructure, making colony morphology a candidate model for understanding how microorganisms interact to form complex structures.

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