Long-term soil metal exposure impaired temporal variation in microbial metatranscriptomes and enriched active phages

BACKGROUND: It remains unclear whether adaptation and changes in diversity associated to a long-term perturbation are sufficient to ensure functional resilience of soil microbial communities. We used RNA-based approaches (16S rRNA gene transcript amplicon coupled to shotgun mRNA sequencing) to study the legacy effects of a century-long soil copper (Cu) pollution on microbial activity and composition, as well as its effect on the capacity of the microbial community to react to temporal fluctuations. RESULTS: Despite evidence of microbial adaptation (e.g., iron homeostasis and avoidance/resistance strategies), increased heterogeneity and richness loss in transcribed gene pools were observed with increasing soil Cu, together with an unexpected predominance of phage mRNA signatures. Apparently, phage activation was either triggered directly by Cu, or indirectly via enhanced expression of DNA repair/SOS response systems in Cu-exposed bacteria. Even though total soil carbon and nitrogen had accumulated with increasing Cu, a reduction in temporally induced mRNA functions was observed. Microbial temporal response groups (TRGs, groups of microbes with a specific temporal response) were heavily affected by Cu, both in abundance and phylogenetic composition. CONCLUSION: Altogether, results point toward a Cu-mediated “decoupling” between environmental fluctuations and microbial activity, where Cu-exposed microbes stopped fulfilling their expected contributions to soil functioning relative to the control. Nevertheless, some functions remained active in February despite Cu, concomitant with an increase in phage mRNA signatures, highlighting that somehow, microbial activity is still happening under these adverse conditions. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40168-018-0606-1) contains supplementary material, which is available to authorized users.