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.

String networks with junctions in competition models

“…Competition models are widely regarded as a crucial tool to understand the mechanisms leading to biodiversity [1][2][3][4] (see also [5,6] for a review). Although the simplest competition models usually consider three species and allow for an equal number of basic microscopic actions (motion, reproduction and predation), many interesting generalizations, including further species and more complex interaction rules, have been considered in the literature In [14,15], a broad family of spatial stochastic May-Leonard models with an arbitrary number of species has been introduced.…”

Predation and selection for antibiotic resistance in natural environments

“…Lytic effects of antibiotics produced can be challenging to observe in experimental settings, because lysis is not always an immediate reaction following exposure to the antibiotic. For example, some bacteriostatic antibiotics are only bacteriocidal after a longer period of exposure (typically measured in days), as observed for bacteriocins produced by lactic acid bacteria (Leisner and Haaber 2012). A delayed lysis of the target cells means that the antibiotics may not have an instant effect, but may secure supply of nutrients at a later stage, for example, when the population bottleneck is more severe.…”

“…A substantial amount of literature exists on the phenomenon of selection for bacterial antibiotic resistance, but the mechanisms underlying its emergence and evolution are still not completely understood (Wright ; Aminov ; Allen et al. ; Davies and Davies ; Leisner and Haaber ; Galan et al. ; Khumbar and Watwe ).…”

“…A substantial amount of literature exists on the phenomenon of selection for bacterial antibiotic resistance, but the mechanisms underlying its emergence and evolution are still not completely understood (Wright 2007;Aminov 2009;Allen et al 2010;Davies and Davies 2010;Leisner and Haaber 2012;Galan et al 2013;Khumbar and Watwe 2013). This uncertainty is also mirrored in a similar lack of consensus on the biological role of antibiotics in nature (Aminov 2009;Martinez 2009;Davies and Davies 2010;Hibbing et al 2010;Galan et al 2013;Sengupta et al 2013).…”

High Levels of Antibiotic Resistance but No Antibiotic Production Detected Along a Gypsum Gradient in Great Onyx Cave, KY, USA

“…The cave microbiome has great potential as a novel resource for drug discovery [5][6][7] due to microbial competition for limited resources. When resources are scarce, microbial production of secondary metabolites including toxins for predation of bacteria on other bacteria [8,9], ionophores, bioregulators, and signal molecules [7] could increase to create a competitive advantage [10,11]. Martinez et al [12] reviewed antibiotic production and resistance, taking a global view that these processes play fundamental ecological roles that shape the structure of microbial communities.…”