Permissive aggregative group formation favors coexistence between cooperators and defectors in yeast

• Published in: The ISME Journal Vol. 16; no. 10; pp. 2305 - 2312
• Main Authors: Belpaire, Tom E. R., Pešek, Jiří, Lories, Bram, Verstrepen, Kevin J., Steenackers, Hans P., Ramon, Herman, Smeets, Bart
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 01.10.2022; Nature Publishing Group
• Subjects: 13/31; 14/3; 631/158/855; 631/326/2565/855; Biomedical and Life Sciences; Cooperation; Ecology; Evolutionary Biology; FLO1 gene; Flocculation; Kin recognition; Life Sciences; Microbial Ecology; Microbial Genetics and Genomics; Microbiology; Political asylum; Recognition; Stability; Yeasts
• ISSN: 1751-7362; 1751-7370
• DOI: 10.1038/s41396-022-01275-y

In Saccharomyces cerevisiae , the FLO1 gene encodes flocculins that lead to formation of multicellular flocs, that offer protection to the constituent cells. Flo1p was found to preferentially bind to fellow cooperators compared to defectors lacking FLO1 expression, enriching cooperators within the flocs. Given this dual function in cooperation and kin recognition, FLO1 has been termed a “green beard gene”. Because of the heterophilic nature of the Flo1p bond however, we hypothesize that kin recognition is permissive and depends on the relative stability of the FLO1 + / flo1 − versus FLO1 + / FLO1 + detachment force F . We combine single-cell measurements of adhesion, individual cell-based simulations of cluster formation, and in vitro flocculation to study the impact of relative bond stability on the evolutionary stability of cooperation. We identify a trade-off between both aspects of the green beard mechanism, with reduced relative bond stability leading to increased kin recognition at the expense of cooperative benefits. We show that the fitness of FLO1 cooperators decreases as their frequency in the population increases, arising from the observed permissive character ( F +−  = 0.5  F ++ ) of the Flo1p bond. Considering the costs associated with FLO1 expression, this asymmetric selection often results in a stable coexistence between cooperators and defectors.