Effects of Three Pesticides on the Earthworm Lumbricus terrestris Gut Microbiota

Abstract

Earthworms play a vital role in the terrestrial ecosystem functioning and maintenance of soil fertility. However, many pesticides, for example, imidacloprid, benomyl, and metribuzin that are world-widely used in agriculture, may be potentially dangerous to earthworms. At the same time, standard tests for pesticides acute and chronic toxicity do not reflect all aspects of their negative impact and might not be enough sensitive for effective assessment. 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 applied 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. Moreover, the pesticides affected the abundance of Verminephrobacter—the earthworms’ nephridia specific symbionts. In general, the negative impact of pesticides on bacterial biodiversity was significant even under pesticides content, which was much lower than their acute and chronic toxicity values for the earthworms. These results highlighted the fact that the earthworm’s gut microbial community is highly sensitive to soil contamination with pesticides. Therefore, such examination should be considered in the pesticide risk assessment protocols.

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

“…Among visible effects, ethyl parathion produced (i) a temporary decrease of soil microbial abundances, (ii) an increase of the gut micro-eukaryotic diversity and (iii) a decrease of casts microbial abundances and diversity that expressed more importantly with the G-soil. Other studies have shown contradictory effects of pesticides on gut microbiota: imidacloprid (neonicotinoid), benomyl (fungicide) and metribuzin (herbicide) were shown to reduce the total prokaryotic diversity in the earthworm's gut (Astaykina et al, 2022). However, we can assume that the soil texture could affect the response of microbial communities as a weak restoration of enzyme activities was observed after parathion exposure in casts from soil G (Jouni et al, 2023).…”

“…Although the gut microbiota has been shown to contribute to host gut, metabolic, and immune homeostasis (Devkota and Chang, 2013), the interest in the role of the gut microbiota in pesticide-induced toxicity in non-target organisms is limited to insects and vertebrates (Giambo et al, 2021;Siddiqui et al, 2022). The few studies that have considered the role of earthworm gut microbiota in the response to pesticides inputs revealed that a gut prokaryotic isolate could degrade Endosulfan in vitro (Verma et al, 2006), that earthworms may filter out bacterial degraders of the herbicide 4-chloro-2methylphenoxyacetic acid (Liu et al, 2013) or that some gut microbial groups were particularly sensitive to various pesticides (Ma et al, 2017;Astaykina et al, 2022), calling for standard consideration of the earthworm gut microbiota in pesticide risk assessment protocols.…”

Earthworms Exposed to Polyethylene and Biodegradable Microplastics in Soil: Microplastic Characterization and Microbial Community Analysis

“…33,34 In this study we investigated microplastics effects on microbial communities in L. terrestris. Previously, it has been reported that the presence of pesticides can alter microbial diversity and composition of L. terrestris, 36 and also, specific diet (beech litter) can cause changes in the gut microbiome. 37 However, our study showed no significant effect on gut microbiome due to microplastics application.…”