Combined effect of bioaugmentation and bioturbation on atrazine degradation in soil

Earthworms, because they change soil physical and chemical properties, are efficient engineers that act on soil microbial community and activity. Thus they may drive pollutant biodegradation in soil such as atrazine mineralization. We hypothesized that earthworms modify the abundance of indigenous soil bacteria and the fate and activity of atrazine-degraders in the soil they engineer by bioturbation. Two bacterial strains were used as bioaugmentation agents: Pseudomonas sp. ADP and Chelatobacter heintzii, which have acquired the capacity to metabolize atrazine by carrying plasmidic atz A, B, C, D, E, F and atzA, B, C, trzD genes, respectively. We analyzed the interactions between earthworms (Lumbricus terrestris) and the indigenous and atrazine-degrading (indigenous and inoculated) bacterial communities by quantifying the 16S rRNA and the atzA gene sequence copies numbers, respectively, in different earthworm microsites. The kinetics of atrazine mineralization were measured to link the bacterial community changes with the degradation function. Digestion by earthworms significantly impacted the number of indigenous bacteria and atrazine mineralization in bioaugmented soils. Regarding the fate of the two atrazine-degraders tested, Pseudomonas sp. strain ADP survived better within the 10 days of experiment than C. heintzii in the bulk soil but the surviving fraction of C. heintzii was still metabolically active and able to mineralize atrazine. A positive “burrow-lining” effect on the atzA sequence copies number was observed in soil whether bioaugmented with C. heintzii or not (i.e. native indigenous atzA) thereby indicating that burrow-linings form a specific ‘hot spot’ for atrazine-degraders. The present study is the first to report the role of earthworms in selecting native catabolic key-genes in soil (indigenous atzA). This catabolic gene selection through earthworm soil bioturbation could be important in sustaining the degradation (detoxification) function of soil.