The Whi2p-Psr1p/Psr2p complex regulates interference competition and expansion of cells with competitive advantage in yeast colonies

Abstract

<jats:p>Yeast form complex highly organized colonies in which cells undergo spatiotemporal phenotypic differentiation in response to local gradients of nutrients, metabolites, and specific signaling molecules. Colony fitness depends on cell interactions, cooperation, and the division of labor between differentiated cell subpopulations. Here, we describe the regulation and dynamics of the expansion of papillae that arise during colony aging, which consist of cells that overcome colony regulatory rules and disrupt the synchronized colony structure. We show that papillae specifically expand within the U cell subpopulation in differentiated colonies. Papillae emerge more frequently in some strains than in others. Genomic analyses further revealed that the Whi2p-Psr1p/Psr2p complex (WPPC) plays a key role in papillae expansion. We show that cells lacking a functional WPPC have a sizable interaction-specific fitness advantage attributable to production of and resistance to a diffusible compound that inhibits growth of other cells. Competitive superiority and high relative fitness of<jats:italic>whi2</jats:italic>and<jats:italic>psr1psr2</jats:italic>strains are particularly pronounced in dense spatially structured colonies and are independent of TORC1 and Msn2p/Msn4p regulators previously associated with the WPPC function. The WPPC function, described here, might be a regulatory mechanism that balances cell competition and cooperation in dense yeast populations and, thus, contributes to cell synchronization, pattern formation, and the expansion of cells with a competitive fitness advantage.</jats:p>

Genetic interaction network has a very limited impact on the evolutionary trajectories in continuous culture-grown populations of yeast

“…This finding was confirmed in the study of Szamecz et al [8], who found that the WHI2 deletion is very weakly deleterious; these researchers also found a compensatory effect of WHI2 inactivation during evolution of a rpb9Δ strain. In contrast, in other environmental conditions (in dense colonies and upon nutrient deprivation), deletion of WHI2 is beneficial [67]. In unstable landscapes, loss-of-function mutations of WHI2 are frequently observed [68].…”

The leucine-NH4+ uptake regulator Any1 limits growth as part of a general amino acid control response to loss of La protein by fission yeast

“…Although sla1Δ cells are deficient for leucine uptake, their slow growth can not be overcome by increasing the concentration of leucine in EMM, consistent with it its uptake inhibitition by NH4 + [50]. A striking characteristic was an apparent communal effect of the SSR mutants on the growth of their otherwise isogenic neighbors [95,96]. As the SSRs emerged as rare mutants from the sla1Δ cells they were surrounded by smaller sattelite colonies (Fig 3A and 3B).…”

Mitochondrial Retrograde Signaling Contributes to Metabolic Differentiation in Yeast Colonies

“…To obtain images of whole colonies we combined two images from neighboring fields of view. For fluorescence microscopy, thin sections were prepared from colonies embedded in 3% agarose using a Leica VT1200S vibrating microtome (Leica, Wetzlar, Germany) [ 14 , 47 ] and observed by an Axio Observer.Z1 fluorescence microscope (Carl Zeiss, Oberkochen, Germany) equipped with an Axiocam 506 and an Apochromat 10×/0.45W objective or an Apochromat 63×/1.20 W using ZEN 2012 (blue edition) software. Filter sets for GFP fluorescence: 450–490 nm and 500–550 nm for excitation and emission, respectively.…”