Abstract

Though traditionally perceived as weapons, antibiotics are also hypothesized to act as microbial signals in natural habitats. However, while subinhibitory concentrations of antibiotics (SICA) are known to shift bacterial gene expression, specific hypotheses as to how SICA influence the ecology of natural populations are scarce. We explored whether antibiotic ‘signals’, or SICA, have the potential to alter nutrient utilization, niche overlap, and competitive species interactions among Streptomyces populations in soil. For nine diverse Streptomyces isolates, we evaluated nutrient utilization patterns on 95 different nutrient sources in the presence and absence of subinhibitory concentrations of five antibiotics. There were significant changes in nutrient use among Streptomyces isolates, including both increases and decreases in the capacity to use individual nutrients in the presence vs. in the absence of SICA. Isolates varied in their responses to SICA and antibiotics varied in their effects on isolates. Furthermore, for some isolate-isolate-antibiotic combinations, competition-free growth (growth for an isolate on all nutrients that were not utilized by a competing isolate), was increased in the presence of SICA, reducing the potential fitness cost of nutrient competition among those competitors. This suggests that antibiotics may provide a mechanism for bacteria to actively minimize niche overlap among competitors in soil. Thus, in contrast to antagonistic coevolutionary dynamics, antibiotics as signals may mediate coevolutionary displacement among coexisting Streptomyces, thereby hindering the emergence of antibiotic resistant phenotypes. These results contribute to our broad understanding of the ecology and evolutionary biology of antibiotics and microbial signals in nature.

Highlights

  • Antibiotic-producing bacteria are common in natural habitats, yet the roles of antibiotics in the ecology and evolutionary biology of soil populations remain poorly understood

  • The Streptomyces isolates used were collected from diverse natural habitats: 1232.2, 3211.5, and 5111.5 were from a prairie in the central USA, Cev2-10 was from a rocky hillside in southwestern France, Lub2-11b was from a forested area in south-central France, Mont3-8 was from a forest in eastern Spain, NZ816-12 was from a beach forest on the South Island of New Zealand, Pan FS14 was from a forested site in central Panama, and Witz25 was from a forested hillside in west-central Germany (Table S1)

  • Shifts in nutrient use in response to subinhibitory concentrations of antibiotics (SICA) were consistent among replicates for each isolate-antibiotic combination, but varied widely among isolates and antibiotics (Figure 1)

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Summary

Introduction

Antibiotic-producing bacteria are common in natural habitats, yet the roles of antibiotics in the ecology and evolutionary biology of soil populations remain poorly understood. Our lack of understanding of the specific roles of antibiotics in natural populations constrains our abilities to identify habitats or selective conditions most likely to generate novel antibiotic phenotypes and to predict the dynamics of antibiotic resistance in environmental microbes. Antibiotics are assumed to mediate antagonistic interactions in soil [11], and antibiotic-producing microbes have been suggested to exhibit coevolutionary arms race dynamics [12]. The arms race model predicts reciprocal accumulation of matching antibiotic inhibitory and resistance capacities in interacting populations over time, with ongoing selection for resistance in the presence of antibioticproducers. If antibiotics mediate signaling interactions, there may be little reason to expect ongoing selection for resistance, suggesting the potential for fundamentally different coevolutionary dynamics. Specific mechanisms by which antibiotic signals may facilitate non-antagonistic interactions remain predominantly hypothetical

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