Invertebrates gut viromes mediate microbial adaptation to pharmaceutical diversity under warming

Pharmaceutical pollution is an emerging environmental concern that can disrupt microbial communities and ecological processes, while climate warming adds further stress with broad ecological consequences. Soil invertebrates such as collembolans harbor gut microbiomes essential for host health and ecosystem stability, yet the responses of these communities-particularly viral communities-to combined pharmaceutical and warming pressures remain unclear. Here, we used controlled microcosm experiments with Folsomia candida to investigate how pharmaceutical diversity and fluctuating warming jointly shape gut microbiomes through bacteria-virus interactions.

Pharmaceutical diversity significantly reduced the alpha diversity of gut viral communities in F. candida, an effect not observed in surrounding soils. Diurnal warming increased the proportion of lysogenic phages and enhanced auxiliary metabolic genes (AMGs) such as ACADM and nrdA. Functional validation in Escherichia coli BL21 confirmed that these genes mitigate oxidative stress and improve host thermal tolerance. In contrast, diverse pharmaceuticals increased the proportion of lytic phages, likely driving nutrient turnover through a "kill-the-winner" dynamic that stimulated bacterial taxa involved in pharmaceutical degradation. Moreover, warming amplified the disruption of gut bacterial communities caused by pharmaceutical diversity and strengthened bacteria-virus co-occurrence networks.

Our findings reveal that gut viruses act as pivotal regulators of microbial adaptation under concurrent chemical and climate stressors. By mediating host resilience and microbial dynamics, the gut virome provides mechanistic insights into ecosystem stability, and may also serve as an early indicator of combined pharmaceutical and warming stress in soil invertebrate systems, underscoring the need to integrate viral-microbial interactions into One Health framework for environmental risk assessment. Video Abstract.