Endocrine disrupting activity in sewage sludge: Screening method, microbial succession and cost-effective strategy for detoxification

Dânia Elisa C Mazzeo; Andrea Dombrowski; Flávio Andrade Oliveira; Carlos Emílio Levy; Jörg Oehlmann; Mary Rosa R Marchi

doi:10.1016/j.jenvman.2022.117207

Endocrine disrupting activity in sewage sludge: Screening method, microbial succession and cost-effective strategy for detoxification

J Environ Manage. 2023 Mar 15:330:117207. doi: 10.1016/j.jenvman.2022.117207. Epub 2023 Jan 6.

Authors

Dânia Elisa C Mazzeo¹, Andrea Dombrowski², Flávio Andrade Oliveira³, Carlos Emílio Levy³, Jörg Oehlmann², Mary Rosa R Marchi⁴

Affiliations

¹ Department of Biotechnology and Plant and Animal Production, Center for Agricultural Sciences, Federal University of São Carlos - UFSCAR, Araras, Brazil. Electronic address: daniamazzeo@ufscar.br.
² Department Aquatic Ecotoxicology, Goethe University Frankfurt am Main, Germany.
³ Department of Clinical Pathology, Faculty of Medical Sciences, State University of Campinas - UNICAMP, Rua Alexander Fleming, 105, 13081-970, Campinas, SP, Brazil.
⁴ Department of Analytical Chemistry, Institute of Chemistry, UNESP - Univ Estadual Paulista, Araraquara, SP, Brazil.

PMID: 36621316
DOI: 10.1016/j.jenvman.2022.117207

Abstract

Sewage sludge (SS) presents a high agronomic potential due to high concentrations of organic matter and nutrients, encouraging its recycling as a soil conditioner. However, the presence of toxic substances can preclude this use. To enable the safe disposal of this waste in agriculture, SS requires additional detoxification to decrease the environmental risks of this practice. Although some alternatives have been proposed in this sense, little attention is provided to eliminating endocrine-disrupting chemicals (EDCs). To fill this gap, this study aimed to develop effective and low-cost technology to eliminate EDCs from SS. For this, a detoxification process combining microorganisms and biostimulating agents (soil, sugarcane bagasse, and coffee grounds) was performed for 2, 4, and 6 months with aerobic and anaerobic SSs. The (anti-)estrogenic, (anti-)androgenic, retinoic-like, and dioxin-like activities of SSs samples were verified using yeast-based reporter-gene assays to prove the effectiveness of the treatments. A fractionation procedure of samples, dividing the target sample extract into several fractions according to their polarity, was conducted to decrease the matrix complexity and facilitate the identification of EDCs. A decrease in the abundance and microbial diversity of the SS samples was noted along the biostimulation with the predominance of filamentous fungal species over yeasts and gram-positive bacteria and non-fermenting rods over enterobacteria. Among the 9 EDCs quantified by LC-ESI-MS/MS, triclosan and alkylphenols presented the highest concentrations in both SS. Before detoxification, the studied SSs induced significant agonistic activity, especially at the human estrogen receptor α (hERα) and the human aryl hydrocarbon receptor (AhR). The raw anaerobic sludge also activated the androgen (hAR), retinoic acid (RARα), and retinoid X (RXRα) receptors. However, no significant endocrine-disrupting activities were observed after the SS detoxification, showing that the technology applied here efficiently eliminates receptor-mediated toxicity.

Keywords: Biostimulation; Chemical fractionation; Endocrine disruptors; Receptor-mediated toxicity; Waste management; in vitro bioassay.

MeSH terms

Cellulose
Cost-Benefit Analysis
Endocrine Disruptors* / analysis
Humans
Saccharum*
Sewage / chemistry
Soil
Tandem Mass Spectrometry
Water Pollutants, Chemical* / chemistry

Substances

Sewage
Cellulose
Water Pollutants, Chemical
Endocrine Disruptors
Soil