Effects of three pesticides on the earthworm Lumbricus terrestris gut microbiota

The activity of earthworms is vital for the soil ecosystem functioning and the maintenance soil fertility. Pesticides imidacloprid, benomyl and metribuzin that are widely used in agriculture are known to be potentially dangerous to earthworms. At the same time, standard tests for pesticides acute and chronic toxicity do not reflect all aspects of its negative impact on earthworms and are not sufficiently sensitive. In this paper we studied the effects of non-lethal concentrations of imidacloprid, benomyl, and metribuzin on the gut bacterial community of Lumbricus terrestris using high-throughput sequencing approach. We found that pesticides reduced the total bacterial diversity in the earthworm's gut even at the recommended application rate. Under the influence of the pesticides, the structure of the gut prokaryotic community underwent changes in the relative abundance of the phyla Proteobacteria, Actinobacteria, Acidobacteria, Planctomyces, Verrucomicrobia, and Cyanobacteria, as well as the genera Haliangium, Gaiella, Paenisporosarcina, Oryzihumus, Candidatus Udaeobacter and Aquisphaera. The pesticides affected specific symbionts of the earthworms such as Verminephrobacter. In general, the impact of pesticides was most significant at an imidacloprid content of 0.0002 mg/kg, metribuzin content of 0.008 mg/kg, and benomyl content of 0.01 mg/kg, which is much lower than the values of acute and chronic toxicity of these pesticides for earthworms. These results unravel the fact that the earthworm's gut microbial community is highly sensitive to soil contamination with pesticides. Therefore, such studies should be included in the pesticide risk assessment for earthworms.