Socially mediated induction and suppression of antibiosis during bacterial coexistence

Abstract

Despite their importance for humans, there is little consensus on the function of antibiotics in nature for the bacteria that produce them. Classical explanations suggest that bacteria use antibiotics as weapons to kill or inhibit competitors, whereas a recent alternative hypothesis states that antibiotics are signals that coordinate cooperative social interactions between coexisting bacteria. Here we distinguish these hypotheses in the prolific antibiotic-producing genus Streptomyces and provide strong evidence that antibiotics are weapons whose expression is significantly influenced by social and competitive interactions between competing strains. We show that cells induce facultative responses to cues produced by competitors by (i) increasing their own antibiotic production, thereby decreasing costs associated with constitutive synthesis of these expensive products, and (ii) by suppressing antibiotic production in competitors, thereby reducing direct threats to themselves. These results thus show that although antibiotic production is profoundly social, it is emphatically not cooperative. Using computer simulations, we next show that these facultative strategies can facilitate the maintenance of biodiversity in a community context by converting lethal interactions between neighboring colonies to neutral interactions where neither strain excludes the other. Thus, just as bacteriocins can lead to increased diversity via rock-paper-scissors dynamics, so too can antibiotics via elicitation and suppression. Our results reveal that social interactions are crucial for understanding antibiosis and bacterial community dynamics, and highlight the potential of interbacterial interactions for novel drug discovery by eliciting pathways that mediate interference competition.

Biofilm formation and toxin production provide a fitness advantage in mixed colonies of environmental yeast isolates

“…Under certain conditions, warfare‐producing and sensitive lineages can coexist within an expanding spatially structured community (Abrudan et al., 2015; Bucci, Nadell, & Xavier, 2011; Gardner & West, 2004; Tait & Sutherland, 2002; Weber, Poxleitner, Hebisch, Frey, & Opitz, 2014). It has also recently been demonstrated that in a dense, well‐mixed community, a warfare phenotype can generate spatial segregation of producing and sensitive lineages (McNally et al., 2017).…”

Antibiotics and the art of bacterial war

“…In addition to up-regulation of attacks, there is also the suggestion of evolved defense strategies in the data from Abrudan et al (4). Strains that made antibiotics when alone were commonly suppressed when grown next to another strain.…”

“…However, several papers have argued that many antibiotics at their low, ecologically relevant concentrations are, in fact, friendly signals that coordinate community functions (3). A study in PNAS by Abrudan et al (4) challenges this view, focusing on 13 natural bacterial strains from the most famous genus of antibiotic producers, Streptomyces. The authors seek to firmly reestablish antibiotic production and regulation in terms of the logic of attack and defense.…”

“…One way is to sense (4). The authors studied how well a focal strain (green) inhibited an overlain target strain (gray box) when growing in the absence, or presence, of a modifier strain (blue).…”

Mining into interspecific bacterial interactions

“…However, the frequency of interaction-mediated antibiotic triggering in bacterial communities was unknown and to date most studies on interactions altering antibiotic production are focused mainly on Streptomyces spp. (Ueda et al, 2000;Traxler et al, 2013;Kinkel et al, 2014;Abrudan et al, 2015).…”