Bacterial adaptation to sublethal antibiotic gradients can change the ecological properties of multitrophic microbial communities

Background/Question/Methods

Antibiotics leak constantly into environments due to widespread use in agriculture and human therapy. Although sublethal concentrations are well known to select for antibiotic resistant bacteria, little is known about how bacterial evolution cascades through food webs, having indirect effect on species not directly affected by antibiotics.

We were interested in answering questions regarding to the selection of sublethal antibiotic concentrations on food webs consisted of bacterial prey and two protist and one phage enemy. We used fully factorial design and modified the mean, variance and autocorrelation structure of the antibiotic concentration in multi-habitat-patch communities that were connected or unconnected via migration in different treatments. We quantified species population dynamics continuously during the experiment and measured how bacterial fitness responded to the antibiotic and to all enemies at the end of the experiment.

We concentrated on answering four broad questions. First, does spatial and temporal variation in sublethal antibiotic concentration select for bacteria with increased growth in the presence of antibiotics? Second, do bacteria evolve defences against enemies of the community? Third, does antibiotic selection interact with anti-predatory defence selection? Fourth, does bacterial response to antibiotics reverberate through food webs, having indirect effects on the ecology of whole microbial community?

Results/Conclusions

We found that selection by sublethal antibiotic concentrations affected bacterial adaptation leading to changes in the ecology of multitrophic microbial communities via secondary effect on species not directly affected by antibiotics. Overall, mean antibiotic concentration and migration affected bacterial evolution, while temporal antibiotic fluctuations affected mainly species’ population dynamics. Even though increasing antibiotic concentration initially increased the mortality of the ancestral bacterium, bacteria evolved to grow better in the presence of antibiotics in all of the antibiotic environments. Furthermore, bacteria evolved defences to all enemies and the highest fitness increases both to antibiotics and to protists occurred in the high antibiotic environment, which is indicative of positive pleiotropy. Finally, the ecological changes in enemy communities were clearest in the high antibiotic concentration environment, which had an overall decrease in predator densities, reduced enemy community diversity and increased temporal fluctuations of bacterial and enemy populations.

Our results show that the presence of natural enemies can modify and even reverse the effects of antibiotics on bacteria, and that antibiotic selection can change the ecological properties of multitrophic microbial communities by having indirect effects on species not directly affected by antibiotics. Leaking of antibiotics could thus have far-reaching, community-wide effects in microbial foodwebs.