Maintenance of Microbial Cooperation Mediated by Public Goods in Single- and Multiple-Trait Scenarios

Abstract

Microbes often form densely populated communities, which favor competitive and cooperative interactions. Cooperation among bacteria often occurs through the production of metabolically costly molecules produced by certain individuals that become available to other neighboring individuals, called public goods. This type of cooperation is susceptible to exploitation, since non-producers of a public good can benefit from it while saving the cost of its production (cheating), gaining a fitness advantage over producers (cooperators). Thus, in mixed cultures, cheaters can increase in frequency in the population, relative to cooperators. Sometimes, and as predicted by simple game-theoretic arguments, such increase in the frequency of cheaters causes loss of the cooperative traits by exhaustion of the public goods, eventually leading to a collapse of the entire population. In other cases, however, both cooperators and cheaters remain in coexistence. This raises the question of how cooperation is maintained in microbial populations. Several strategies to prevent cheating have been described involving a single trait and a unique environmental constraint. In this review, we describe current knowledge on the evolutionary stability of microbial cooperation, discussing recent discoveries describing the mechanisms operating in multiple traits and multiple constraints settings. We conclude with a consideration of the consequences of these complex interactions, and we briefly discuss the potential role of social interactions involving multiple traits and multiple environmental constraints in the evolution of specialization and division of labor in microbes.

An evolutionary quantitative genetics model for phenotypic (co)variances under limited dispersal, with an application to socially synergistic traits

“…); in microorganisms, each trait could be the production of a specific amino acid that is released into the external environment from which it can then be absorbed and used by group members (e.g., Özkaya et al. ).…”

“…We model the coevolution of two nonnegative quantitative traits, labeled 1 and 2, that each capture participation to a different public good. For example, in group living mammals, one trait could be the time/energy invested into foraging for the group's offspring, and the other, investment into defending the group by standing sentry against predators (e.g., Carter et al 2014); in microorganisms, each trait could be the production of a specific amino acid that is released into the external environment from which it can then be absorbed and used by group members (e.g., Ozkaya et al 2017).…”

Genetic architecture constrains exploitation of siderophore cooperation in the bacteriumBurkholderia cenocepacia

“…; Bruger and Waters ; Özkaya et al. ). Here, we studied siderophore production in B. cenocepacia H111 and found that patterns of siderophore sharing and exploitation can be very different from the ones reported for P. aeruginosa .…”

“…; Özkaya et al. ). A large body of work has tackled this question and revealed that cheating and cheater control are major determinants of bacterial population dynamics in host infections, in laboratory experiments, and in environmental communities (Cordero et al.…”

A quantitative genetics approach to the evolution of phenotypic (co)variance under limited dispersal, with an application to socially synergistic traits

“…Another pair of traits whose evolution is likely to be influenced by their joint expression in different individuals is the production and exploitation of a public good, such as the secretion and use of siderophores by microorganisms (West et al, 2006). Under limited diffusion of siderophores and limited bacterial dispersal (Nadell et al, 2009, Kümmerli et al, 2014, Ross-Gillespie et al, 2015, we expect kin selection effects to be ecologically relevant for how secretion and use of siderophores are associated, and more generally for patterns of multi-trait social variation within microbial communities (Cordero and Polz, 2014, van Gestel et al, 2015, Özkaya et al, 2017, Schiessl et al, 2019, Rodríguez Amor and Dal Bello, 2019.…”