Individual‐ versus group‐optimality in the production of secreted bacterial compounds

Abstract

How unicellular organisms optimize the production of compounds is a fundamental biological question. While it is typically thought that production is optimized at the individual-cell level, secreted compounds could also allow for optimization at the group level, leading to a division of labor where a subset of cells produces and shares the compound with everyone. Using mathematical modelling, we show that the evolution of such division of labor depends on the cost function of compound production. Specifically, for any trait with saturating benefits, linear costs promote the evolution of uniform production levels across cells. Conversely, production costs that diminish with higher output levels favor the evolution of specialization – especially when compound shareability is high. When experimentally testing these predictions with pyoverdine, a secreted iron-scavenging compound produced by Pseudomonas aeruginosa, we found linear costs and, consistent with our model, detected uniform pyoverdine production levels across cells. We conclude that for shared compounds with saturating benefits, the evolution of division of labor is facilitated by a diminishing cost function. More generally, we note that shifts in the level of selection from individuals to groups do not solely require cooperation, but critically depend on mechanistic factors, including the distribution of compound synthesis costs.

Pseudomonas aeruginosareaches collective decisions via transient segregation of quorum sensing activities across cells

“…While the growth conditions in our experiment were rather uniform (shaken cultures), there is still potential for stochasticity. For example, there might be stochastic inter-cell differences in nutrient uptake, which can spur variation in metabolic states across cells and induce heterogeneity in overall gene expression activity 44,45 . Moreover, the very nature of QS systems operating via diffusible signals can promote extrinsic noise.…”

From heterogeneity to homogeneity: coordination of siderophore gene expression among clonal cells of the bacteriumPseudomonas aeruginosa

“…One extreme answer could be that there is no coordination and that the observed population level responses [30][31][32] might merely be the sum of its heterogenous individual members. Conversely, it could be that the regulatory circuits operate in a way that fosters specialization [33], where fractions of cells in a population invest either in pyochelin or pyoverdine.…”

Evolution of specialized microbial cooperation in dynamic fluids

“…Existing computational models of evolution of specialization that consider spatial structure or finite group size typically abstract away the underlying physics (Cooper & West, ; Gavrilets, ; Ispolatov, Ackermann, & Doebeli, ; Menon & Korolev, ; Oliveira, Niehus, & Foster, ; Rueffler et al, ; Schiessl et al, ; Vural et al, ; Willensdorfer, ). While conceptually useful, such models reveal little about the interplay between evolutionary and mechanical forces during the formation and evolution of specialization.…”