Eco-evolutionary dynamics and environmental detoxification jointly shape bacterial community response to antibiotic perturbation.

Microbial communities frequently encounter recurrent antibiotic disturbance, yet how ecological, evolutionary, and environmental processes jointly shape community responses remains unresolved. Here, we use priming to describe the history-dependent effect whereby prior exposure alters the response to a subsequent disturbance. Using a 23-species bacterial community exposed to sequential ampicillin pulses, we examined two dimensions of priming. The ecological dimension was manipulated by exposing assembled communities to an antibiotic pre-pulse that could alter species composition before a common high-dose pulse. The evolutionary dimension was manipulated by experimentally evolving individual species for increased ampicillin resistance before community assembly. Community-level pre-pulse exposure shifted composition toward resistant taxa before the main disturbance, reducing subsequent compositional change. Prior resistance evolution had the strongest effect on community dynamics, buffering compositional change during the main pulse, relaxing subsequent selection, and altering community-wide gene expression. This buffering arose from both increased resistance within species and accelerated ampicillin detoxification by a dominant degrader, which transiently reduced antibiotic exposure and promoted the persistence of non-degrading taxa. However, greater resistance did not improve recovery. Because resistance was coupled to competitive dominance, diversity after disturbance remained similar to or lower than in ancestral communities, whereas dominant taxa became further enriched. Together, our results show that antibiotic exposure history reshapes microbial disturbance responses through interacting eco-evolutionary and environmental feedbacks. These feedbacks increase resistance to recurrent disturbance but can constrain recovery, revealing a trade-off between resistance and diversity restoration.