A novel concept for the biodegradation mechanism of dianionic catechol with homoprotocatechuate 2,3-dioxygenase: A non-proton-assisted process

Ningyu Tu; Dongmei Zhang; Xianchun Niu; Cheng Du; Li Zhang; Wenyu Xie; Xiaojun Niu; Yang Liu; Youming Li

doi:10.1016/j.chemosphere.2019.125796

A novel concept for the biodegradation mechanism of dianionic catechol with homoprotocatechuate 2,3-dioxygenase: A non-proton-assisted process

Chemosphere. 2020 May:246:125796. doi: 10.1016/j.chemosphere.2019.125796. Epub 2019 Dec 30.

Authors

Ningyu Tu¹, Dongmei Zhang¹, Xianchun Niu¹, Cheng Du¹, Li Zhang¹, Wenyu Xie¹, Xiaojun Niu², Yang Liu³, Youming Li⁴

Affiliations

¹ School of Environmental Science and Engineering, Guangdong University of Petrochemical Technology, Maoming, Guangdong, 525000, China; Guangdong Provincial Key Laboratory of Petrochemical Pollution Process and Control, Guangdong University of Petrochemical Technology, Maoming, 525000, China.
² School of Environmental Science and Engineering, Guangdong University of Petrochemical Technology, Maoming, Guangdong, 525000, China; Guangdong Provincial Key Laboratory of Petrochemical Pollution Process and Control, Guangdong University of Petrochemical Technology, Maoming, 525000, China; School of Environment and Energy, South China University of Technology, Guangzhou, 510006, China.
³ School of Environmental Science and Engineering, Guangdong University of Petrochemical Technology, Maoming, Guangdong, 525000, China; Guangdong Provincial Key Laboratory of Petrochemical Pollution Process and Control, Guangdong University of Petrochemical Technology, Maoming, 525000, China. Electronic address: liuyang@gdupt.edu.cn.
⁴ State Key Laboratory of Pulp and Paper Engineering, South China University of Technology, Guangzhou, 510640, China.

PMID: 31918103
DOI: 10.1016/j.chemosphere.2019.125796

Abstract

The theory of "proton-assisted process" can well explain the catalytic mechanism of homoprotocatechuate 2,3-dioxygenase (2,3-HPCD) with a monoanionic substrate (homoprotocatechuate, HPCA). Here a "non-proton-assisted process" is presented to interpret catalytic mechanism of 2,3-HPCD with a dianionic substrate (4-nitrocatechol, 4NC). The ONIOM calculation is performed to investigate the reaction pathway of a wild-type 2,3-HPCD with 4NC (H200H-4NC system). The catalytic reaction is comprised of four steps: (1) A dioxygen attacks the aromatic ring to produce an alkylperoxo species. (2) O-O bond cleavage and the formation of an epoxide species occur. (3) A seven-membered O-heterocyclic compound is generated by the extinction of the epoxy structure. (4) The seven-membered ring undergoes ring opening to form the final product (C2-C3 cleavage product). The effective free energy barrier of the catalytic reaction of the H200H-4NC system is 26.2 kcal mol^-1, which is much higher than that of the H200H-HPCA system. Furthermore, two calculated electronic configurations (Fe(III)-O₂^•- and Fe(III)-SQ^•) have a high similarity to previously detected ones, which demonstrates that the Asn200 variant (H200N-4NC variant system) employs a C4 (para-carbon) pathway to produce a C4-C5 cleavage product. Our findings provide an in-depth understanding of the catalytic mechanisms of dianionic catechol and its derivatives.

Keywords: 2,3-HPCD; 4NC; Alkylperoxo species; Catalytic mechanism; Non-proton-assisted process.

MeSH terms

Biodegradation, Environmental*
Catalysis
Catechols / chemistry
Catechols / metabolism*
Dioxygenases / metabolism*
Ferric Compounds
Oxygen / chemistry
Protons

Substances

Catechols
Ferric Compounds
Protons
Dioxygenases
3,4-dihydroxyphenylacetate 2,3-dioxygenase
catechol
Oxygen
4-nitrocatechol