Influence of the geophagous earthworm Aporrectodea sp. on the fate of bisphenol A and a branched 4-nonylphenol isomer in soil

Authors: SHAN, JUN - Chinese Academy Of Sciences; CORVINI, PHILIPPE FRANCO - Nanjing University; SHAEFFER, ANDREAS - Nanjing University Of Information Science And Technology (NUIST); Chee Sanford, Joanne; YAN, XIAOYUAN - Nanjing University; JI, RONG - Chinese Academy Of Sciences

Submitted to: Science of the Total Environment
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/23/2019
Publication Date: 7/23/2019
Citation: Shan, J., Corvini, P., Shaeffer, A., Chee Sanford, J.C., Yan, X., Ji, R. 2019. Influence of the geophagous earthworm Aporrectodea sp. on the fate of bisphenol A and a branched 4-nonylphenol isomer in soil. Science of the Total Environment. 693:133574. https://doi.org/10.1016/j.scitotenv.2019.07.380.
DOI: https://doi.org/10.1016/j.scitotenv.2019.07.380

Interpretive Summary: Earthworms are known to affect organic contaminants in soil by degradation, influencing adsorption of compounds to clay and soil organic matter, and concentrating compounds in their biomass. Since earthworms are abundant in many soils, their influence on the physicochemical and biological properties of soils can be large, ultimately affecting the fate of important compounds such as pesticides (e.g. atrazine) and pharmaceuticals that enter agricultural soils via biosolids that are applied as fertilizers. In this study, the effects of the earthworm Aporrectodea sp. on two endocrine disrupting chemicals (EDCs), bisphenol A (BPA) and nonylphenol (NP), in soil were measured using 14C labeled compounds to track their fate and the fate of their degradation products. Earthworms did not affect the mineralization of BPA, but did significantly inhibit the binding and the size distribution of BPA residues within the humic fraction of soil. Earthworms significantly inhibited the mineralization and bound residue formation of NP, and promoted the dissipation of NP and its metabolites in soil. After 9 days of incubation, 75% and 46% of the initially applied 14C-BPA and 14C-NP, respectively, were already present in bound residues. Further, accumulations of 14C-BPA or 14C-NP residues in earthworm biomass were predominant (>50%) indicating that risk assessment of EDCs based solely on their free form will lead to significant underestimation. Our results suggested that degradation and transformation of EDCs not only depend on their physicochemical properties, but also were intensively affected by the activities of earthworms through their direct ingestion and excretion of soil, formation of casts, direct/indirect influences on biodegradation mediated by soil microbes, and soil sorption mechanisms. Similar mechanisms of fate mediated by earthworms have been found with compounds like atrazine and a variety of phenolics, the latter that may include herbicidal compounds commonly used in agriculture. The impact of this study further demonstrates the role of earthworms in affecting organic contaminants in soil. The stability of organic compounds and assessments of potential risks these compounds and their metabolites have in soil ecosystems need to consider the influence of earthworms.

Technical Abstract: Large amounts of endocrine disrupting chemicals (EDCs) including bisphenol A (BPA) and nonylphenol (NP) are released into the soil due to the application of biosolids. Earthworms are the predominant biomass in many terrestrial ecosystems and profoundly influence the physico-chemical and biological properties of soils. However, information about the effects of earthworm activities on the behaviors of EDCs in soil is still limited. Here, the effects of earthworm on mineralization, degradation, and bound residue formation of BPA and NP were investigated using the 14C tracer technique. The results showed that earthworms do not affect mineralization of BPA, but significantly inhibited bound residue formation of BPA and changed the size distribution of BPA residues within humic substances. Earthworms significantly inhibited mineralization and bound residue formation of NP, whereas it also significantly promoted the dissipation of NP and NP’s metabolites in soil. After 9 days of incubation, 75% and 46% of the initially applied 14C-BPA and 14C-NP were already present in bound residues, respectively, indicating that the major route of dissipation of BPA and NP in soil was bound-residue formation. Among total 14C-BPA or 14C-NP residues accumulated in earthworms, bound residues were also predominant (>50%), implying that risk assessment of EDCs based on their concentrations of free form in earthworms might be significantly underestimated. Taken together, our results suggest that fate of EDCs in soil not only depended on their physico-chemical properties but also was intensively affected by earthworm activities, underlining that effects of earthworms should be considered when evaluating environmental behavior and potential risk of EDCs in soil.