Major biotransformation of phthalic acid esters in Eisenia fetida: Mechanistic insights and association with catalytic enzymes and intestinal symbionts

Xiuli Fan; Chenggang Gu; Zhihua Jin; Jun Cai; Yongrong Bian; Fang Wang; Hong Chen; Xin Jiang

doi:10.1016/j.envint.2022.107712

Major biotransformation of phthalic acid esters in Eisenia fetida: Mechanistic insights and association with catalytic enzymes and intestinal symbionts

Environ Int. 2023 Jan:171:107712. doi: 10.1016/j.envint.2022.107712. Epub 2022 Dec 23.

Authors

Xiuli Fan¹, Chenggang Gu², Zhihua Jin¹, Jun Cai¹, Yongrong Bian¹, Fang Wang¹, Hong Chen³, Xin Jiang¹

Affiliations

¹ CAS Key Laboratory of Soil Environment and Pollution Remediation, Institute of Soil Science, Chinese Academy of Sciences, Nanjing 210008, PR China; University of the Chinese Academy of Sciences, Beijing 100049, PR China.
² CAS Key Laboratory of Soil Environment and Pollution Remediation, Institute of Soil Science, Chinese Academy of Sciences, Nanjing 210008, PR China; University of the Chinese Academy of Sciences, Beijing 100049, PR China. Electronic address: cggu@issas.ac.cn.
³ State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing 210008, PR China.

PMID: 36577298
DOI: 10.1016/j.envint.2022.107712

Abstract

Phthalic acid esters (PAEs) are an important group of organic pollutants that are widely used as plasticizers in the environment. The PAEs in soil organisms are likely to be biotransformed into a variety of metabolites, and the combined toxicity of PAEs and their metabolites might be more serious than PAEs alone. However, there are only a few studies on PAE biotransformation by terrestrial animals, e.g. earthworms. Herein, the key biotransformation pathways of PAEs and their association with catalytic enzymes and intestinal symbionts in earthworms were studied using in vivo and in vitro incubation approaches. The widely distributed PAE in soil, dibutyl phthalate (DBP), was proven to be biotransformed rapidly together with apparent bioaccumulation in earthworms. The biotransformation of PAE congeners with medium or long side chains appeared to be faster compared with those with short side chains. DBP was biotransformed into butyl methyl phthalate (BMP), monobutyl phthalate (MBP), and phthalic acid (PA) through esterolysis and transesterification. Besides, the generation of small quantities of low-molecular weight metabolites via β-oxidation, decarboxylation or ring-cleavage, was also observed, especially when the appropriate proportion of NADPH coenzyme was applied to transfer electrons for oxidases. Interestingly, the esterolysis of PAEs was mainly regulated by the cytoplasmic carboxylesterase (CarE) in earthworms, with a Michaelis constant (K_m) of 0.416 mM in the catalysis of DBP. The stronger esterolysis in non-intestinal tissues indicated that the CarE was primarily secreted by non-intestinal tissues of earthworms. Additionally, the intestinal symbiotic bacteria of earthworms could respond to PAE stress, leading to the changes in their diversity and composition. The enrichment of some genera e.g. Bacillus and Paracoccus, and the enhancement of metabolism function, e.g. amino acids, energy, lipids biosynthesis and oxidase secretion, indicated their important role in the degradation of PAEs.

Keywords: Biotransformation pathways; Carboxylesterase; DBP; Earthworms; Intestinal bacteria.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Biotransformation
China
Dibutyl Phthalate
Esters / chemistry
Oligochaeta*
Phthalic Acids* / metabolism
Soil / chemistry

Substances

Phthalic Acids
Dibutyl Phthalate
Soil
Esters