Effect of an organophosphorus insecticide, soil texture and earthworm species on the turnover of soil, gut and cast microbiota during the earthworm's gut transit

Abstract

The growing usage of plant protection products in agroecosystems questions their unintentional deleterious effects on non-target organisms such as earthworms and their related ecological function. The aim of this study was to investigate the turnover of soil microbiota during the gut transit of two endogeic earthworms (Aporrectodea caliginosa and Allolobophora chlorotica) and how it is possibly affected by the organophosphorus insecticide ethyl-parathion (Pt). We measured prokaryotic and micro-eukaryotic community composition and abundances using two different soil types in the continuum of bulk soil, gut and casts samples collected during and after one week exposure to Pt. The presence of earthworm and Pt had limited effects on the soil microbiota, although Pt altered temporarily soil microbial abundances in the presence of earthworms, not in their absence. The earthworms’ gut harbored a remarkably low prokaryotic diversity, dominated by two molecular Operational Taxonomic Units (mOTUs) affiliated to Rhodococcus and Pseudarthrobacter. Contrastingly, gut micro-eukaryotic communities were maintained at diversity levels similar to that of the soil, yet Pt augmented their diversity and changed their composition. Fresh casts collected out of the soil revealed evident variation of abundance, diversity and community composition according to the soil origin and the earthworm species. In particular, following gut transit casts were enriched with Bacteroidia and γ-Proteobacteria while depleted of Acidobacteria. Exposure to Pt increased the diversity and relative abundance of depleted mOTUs, which paves the way for future investigations on the role of Pt in rising microbial consumption due to an over-excitation of gastrointestinal motility.