Abstract
We use the budding yeast, Saccharomyces cerevisiae, to investigate one model for the initial emergence of multicellularity: the formation of multicellular aggregates as a result of incomplete cell separation. We combine simulations with experiments to show how the use of secreted public goods favors the formation of multicellular aggregates. Yeast cells can cooperate by secreting invertase, an enzyme that digests sucrose into monosaccharides, and many wild isolates are multicellular because cell walls remain attached to each other after the cells divide. We manipulate invertase secretion and cell attachment, and show that multicellular clumps have two advantages over single cells: they grow under conditions where single cells cannot and they compete better against cheaters, cells that do not make invertase. We propose that the prior use of public goods led to selection for the incomplete cell separation that first produced multicellularity.
Highlights
During evolution, smaller and simpler elements have repeatedly come together to make bigger and more complicated functional units; examples include genes forming genomes and individuals forming societies
Multicellular organisms are societies of cells and the transition from single to multicelled groups arises in two ways [1,2]: (1) single cells come together to form groups that subsequently differentiate into different cell types, or (2) the offspring of a single cell stay stuck together after cell division
Lab Yeast Cannot Grow from a Single Cell in Low Concentrations of Sucrose
Summary
Smaller and simpler elements have repeatedly come together to make bigger and more complicated functional units; examples include genes forming genomes and individuals forming societies. Multicellular organisms are societies of cells and the transition from single to multicelled groups arises in two ways [1,2]: (1) single cells come together to form groups that subsequently differentiate into different cell types (e.g., slime molds and myxobacteria), or (2) the offspring of a single cell stay stuck together after cell division. This second mode—incomplete cell separation—appears to be a critical step in the independent origins of multicellularity that led to animals, plants, and colonial algae [3]. We focus on what was likely to be the initial step in the evolution of multicellularity, the appearance of aggregates of undifferentiated groups of cells, and ignore two crucial later stages common to plants and animals: the division of labor between different cell types and reproduction through single-celled propagules
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