Abstract
BackgroundIt 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.ResultsDespite 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.ConclusionAltogether, 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.
Highlights
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
The present study aims at (i) bringing new knowledge on microbial adaptation mechanisms to persistent and contrasted Cu pollution concentrations, while (ii) deciphering how Cu has influenced the capacity of the soil microbial community to react to environmental fluctuations
We observed the diminution of specific phylogenetic groups in Cu-plots (Additional file 1: Table S2), including Gammaproteobacteria and Actinobacteria, both harboring well-described members involved in active degradation of soil organic matter [24]
Summary
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. Following industrial and agricultural revolutions, the fast development of our societies increased anthropogenic pressure on soils, notably via intensive farming and use of phytosanitary products, such as metal/metalloid derived pesticides Due to their non-degradable nature, these compounds represent an extremely persistent pollution, often accumulating in specific environmental. The recent advances in mRNA sequencing allow direct access to microbial expression profiles, soil metatranscriptomic studies focusing on environmental fluctuations linked to temporal aspects are still scarce [15]. It remains unresolved if soil microbes coping with persistent pollution possess/express sufficient genetic diversity to maintain their functions under ever-fluctuating environmental conditions
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