Abstract
How unicellular organisms optimize the production of compounds (enzymes and metabolites) is a fundamental biological question. While it is typically thought that this production is optimized at the individual cell level, we examine whether it can also be optimized at the group level instead, through specialization, where a fraction of cells secretes and shares compounds with the other group members. Using mathematical modeling, we show that within-group division of labor is promoted if (1) the per-compound production costs diminish with higher production volumes, and (2) compound sharing is sufficiently high. Experiments with pyoverdine, a shareable compound secreted by Pseudomonas aeruginosa, indeed revealed diminishing costs, yet instead of dividing labor, all cells engage in pyoverdine production. We conclude that even when diminishing costs ostensibly favor phenotypic specialization, its evolution can either be hindered by factors limiting reliable compound sharing in the natural environment or mechanistic constraints impeding stochastic or signal-induced heterogeneity to arise. Thus, shifts in the level of selection, from individuals to groups, might be restricted in loose microbial groups.