Environmentally Relevant Concentrations of the Flame Retardant Tris(1,3-dichloro-2-propyl) Phosphate Inhibit the Growth and Reproduction of Earthworms in Soil

Tris(1,3-dichloro-2-propyl) phosphate (TDCIPP) is a synthetic organophosphate flame retardant that has been used for decades in various products. Its environmental occurrence and toxicity to aquatic organisms has been reported. However, no study to date has been performed on the toxicity of TDCIPP to terrestrial invertebrates. In this study, earthworms (Eisenia fetida) were exposed to 0, 50, 500, and 5000 ng/g TDCIPP in soil for 28 d. The 500 and 5000 ng/g TDCIPP treatments significantly lowered (4.2% and 9.2%, respectively) the average body mass of earthworms, and the 5000 ng/g TDCIPP treatments significantly decreased (25.0%) the number of juveniles born per earthworm. Moreover, seminal vesicle injury, skin lesions, and muscle atrophy were observed. It is worth noting that E. fetida accumulated TDCIPP mainly via epidermal adsorption. Using a combination of transcriptomics and metabolomics, detailed molecular information was provided on the responses of earthworms to TDCIPP exposure. After 5000 ng/g TDCIPP exposure, the contents of l-malic acid, cholesterol, scyllo-inositol, d-galactose, and maltose significantly changed, and transcriptomic analysis identified 80 upregulated and 55 downregulated differentially expressed genes compared with the control group. TDCIPP exposure affected the hormone biosynthesis pathway, leading to the inhibition of earthworm reproduction. The inhibition of growth can be attributed to an affected phosphatidylinositol signaling system and the arachidonic acid metabolism pathway. These findings provide new insight into the molecular mechanisms by which earthworms respond to TDCIPP exposure and offer important information for the environmental risk assessment of organophosphate flame retardants.