Intraguild predation provides a selection mechanism for bacterial antagonistic compounds

Abstract

Bacteriocins are bacterial proteinaceous toxins with bacteriostatic or bacteriocidal activity towards other bacteria. The current theory on their biological role concerns especially colicins, with underlying social interactions described as an example of spite. This leads to a rock-paper-scissors game between colicin producers and sensitive and resistant variants. The generality of this type of selection mechanism has previously been challenged with lactic acid bacterial (LAB) bacteriocins as an example. In the natural environment of LAB, batch cultures are the norm opposed to the natural habitats of Escherichia coli where continuous cultures are prevailing. This implies that fitness for LAB, to a large degree, is related to survival rates (bottleneck situations) rather than to growth rates. We suggest that the biological role of LAB bacteriocins is to enhance survival in the stationary growth phase by securing a supply of nutrients from lysed target cells. Thus, this social interaction is an example of selfishness rather than of spite. Specifically, it fits into an ecological model known as intraguild predation (IGP), which is a combination of competition and predation where the predator (LAB bacteriocin producer) and prey (bacteriocin susceptible bacteria) share similar and often limited resources. We hypothesize that IGP may be a common phenomenon promoting microbial production of antagonistic compounds.

Figure 1.

Overview on social models that illustrate distinct types of selection of bacteriocins, (a) the competitive model concerning colicins and (b) the intraguild predation model concerning LAB bacteriocins. P, bacteriocin producer; S, bacteriocin susceptible; R, bacteriocin resistant; -r, related; -u, unrelated. Relatedness is also symbolized by open circles, while un-relatedness is symbolized by grey ovals. In (a) a continuous culture, selection pressure is on high growth rates. In such systems, there is a fitness cost of expressing bacteriocin resistance genes, but an even larger fitness cost of producing bacteriocins (spite). However, the fastest growing bacteriocin susceptible population will be killed by bacteriocins. This phenomenon is described by the rock–paper–scissors model. In (b) a batch culture, selection pressure is shifted towards survival in the bottleneck scenario when resources have been exhausted. Here the cost of producing bacteriocins is outweighed by the benefits gained from uptake of nutrients from the lysed sensitive cells. In situations with a low dispersion factor, resistant and related variants will be selectively favoured, which will not be the case under global conditions.