Aspects of Multicellularity in Saccharomyces cerevisiae Yeast: A Review of Evolutionary and Physiological Mechanisms

Abstract

The evolutionary transition from single-celled to multicellular growth is a classic and intriguing problem in biology. Saccharomyces cerevisiae is a useful model to study questions regarding cell aggregation, heterogeneity and cooperation. In this review, we discuss scenarios of group formation and how this promotes facultative multicellularity in S. cerevisiae. We first describe proximate mechanisms leading to aggregation. These mechanisms include staying together and coming together, and can lead to group heterogeneity. Heterogeneity is promoted by nutrient limitation, structured environments and aging. We then characterize the evolutionary benefits and costs of facultative multicellularity in yeast. We summarize current knowledge and focus on the newest state-of-the-art discoveries that will fuel future research programmes aiming to understand facultative microbial multicellularity.

Keywords: AMN1 gene; adaptation; aging; cell differentiation; cell specialization; cooperation; evolution; facultative multicellularity; metabolic cooperation; spatial structure; starvation; yeast exometabolome.

Figure 1

Mechanisms of cells aggregation (A) and cell differentiation (B) in multicellular yeast populations. (A) Colors symbolize cells′ genetic background. Cell shape reflects successive divisions. Cell aggregates can form by the “stay together” strategy, where daughter cells stay attached to the mother cell, leading to the formation of clonal adhesions. Alternatively, cells separate after each division and can aggregate later by cell wall adhesins (“come together”), leading to the formation of groups with random relations between cells. Both stay together and come together strategies lead to the formation of two aggregates with 16 cells each, but relatedness between adjacent cells differs. (B) There are three major environmental signals causing cell heterogeneity—nutrient limitation (starvation), structured environment and population aging. Initially, identical cells in the population can enter the apoptosis pathway (uneven shape), enter the quiescence pathway (bold outline) or specialize to perform various tasks (cell shape).