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.
Chemical communication among kin bacteria modulates diverse activities. Despite the general consensus that signaling among non-kin organisms is likely to influence microbial behavior, there is limited information on the potential for microbial interactions to alter microbial phenotypes in natural habitats. We explored patterns of interaction that alter inhibitory phenotypes among Streptomyces isolates from distinct communities. Shifts in inhibition in response to the presence of a partner were evaluated for 861 isolate combinations, and were considered in relation to nutrient use, 16S sequence, inhibition phenotype and community origin. The frequency of inhibition-shifting interactions was significantly higher among isolates from the same (0.40) than from different (0.33) communities, suggesting local selection for inhibition-shifting interactions. Communities varied in the frequency with which Streptomyces isolates responded to a partner but not in the frequency with which isolates induced changes in partners. Streptomyces isolates were more likely to exhibit increased inhibition of a target bacterium in response to isolates that compete for the same nutrients, are closely-related or are strongly inhibited by their antibiotics. This work documents a high frequency of interactions among Streptomyces that shift the capacity of Streptomyces to inhibit other microbes, and suggests significant potential for such interactions to shape microbial community dynamics.
Diseases remain a yield-limiting factor for crops despite the availability of control measures for many pathogens. Indigenous soil microorganisms can suppress some plant pathogens, yet there is little systematic information on the effects of cropping systems on disease-suppressive populations in soil. Streptomyces have been associated with suppression of plant diseases in several naturally occurring disease-suppressive soils. Pathogen-suppressive activity of Streptomyces communities is correlated with higher bacterial densities and with inhibitory phenotypes, driven by competition among indigenous soil bacteria. We sought to characterize relationships between cropping practices and pathogen suppression among soil Streptomyces. We evaluated bacterial and Streptomyces densities and inhibitory activities in soils from a long-term crop rotation experiment. Signaling interactions that altered inhibitory phenotypes among sympatric populations were also evaluated for a subset of samples. Soils from longer rotations, which had a higher number of plant species over time, had larger bacterial and Streptomyces densities, and more inhibitors than soils from shorter rotations. In addition, signaling occurred more frequently among isolates from higher-density communities. Our work shows that bacterial density, pathogen suppression and signaling are interrelated and are affected by crop rotation, suggesting the potential for management to optimize suppressive populations.
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