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

Abstract

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 (e.g. via population dynamics or pleiotropic effects). Here, we used an experimental evolution approach to test how temporal patterns of antibiotic stress, as well as migration within metapopulations, affect the evolution and ecology of microcosms containing one prey bacterium, one phage and two protist predators. We found that environmental variability, autocorrelation and migration had only subtle effects for population and evolutionary dynamics. However, unexpectedly, bacteria evolved greatest fitness increases to both antibiotics and enemies when the sublethal levels of antibiotics were highest, indicating positive pleiotropy. Crucially, bacterial adaptation cascaded through the food web leading to reduced predator-to-prey abundance ratio, lowered predator community diversity and increased instability of 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.

Relative importance of evolutionary dynamics depends on the composition of microbial predator–prey community

“…However, we did find that evolved prey populations became less productive compared with non-evolved or control populations. At the colony-type level, reduced growth was linked with specialist and generalist defender prey phenotypes, suggesting that evolving prey defence was traded-off with prey competitive ability, a commonly found trade-off in microbial predator-prey systems (Yoshida et al, 2003;Meyer and Kassen, 2007;Friman and Laakso, 2011;Friman et al, 2015). Such a trade-off could also have affected prey population instability (Abrams, 2000;Yoshida et al, 2003;Ellner and Becks, 2011).…”

On the possible ecological roles of antimicrobials

“…However, antibiotic resistance is not the only adaptation that is being accelerated by antibiotics (Gorini & Kataja, 1964;Nagel & Chan, 2006). For example, antibiotics accelerate evolution of adaptation to phage and protist predation (Friman, Guzman, Reuman, & Bell, 2015). There is no reason to think that antibiotics at subinhibitory concentrations do not accelerate evolution of other traits!…”

Analysing eco‐evolutionary dynamics—The challenging complexity of the real world

“…Others, mainly studies on microbial and unicellular organisms, quantify eco-evolutionary feedbacks as evolution proceeds (Becks, Ellner, Jones, & Hairston, 2012;Fukami et al, 2007;Gómez et al, 2016;Yoshida et al, 2003). Many of these proof-of-principle experiments demonstrate striking effects of evolutionary trait change on population dynamics and composition (Brunner et al, 2017;Fukami et al, 2007), species interactions (Becks et al, 2012;Friman, Guzman, Reuman, & Bell, 2015;Yoshida et al, 2003), community composition (Gómez et al, 2016;Pantel et al, 2015;terHorst et al, 2014) and ecosystem features (Bassar et al, 2010;Harmon et al, 2009).…”