Purple acid phosphatase promoted hydrolysis of organophosphate pesticides in microalgae

Xiang Wang; Guo-Hui He; Zhen-Yao Wang; Hui-Ying Xu; Jin-Hua Mou; Zi-Hao Qin; Carol Sze Ki Lin; Wei-Dong Yang; Yalei Zhang; Hong-Ye Li

doi:10.1016/j.ese.2023.100318

Purple acid phosphatase promoted hydrolysis of organophosphate pesticides in microalgae

Environ Sci Ecotechnol. 2023 Sep 22:18:100318. doi: 10.1016/j.ese.2023.100318. eCollection 2024 Mar.

Authors

Xiang Wang^{1

2}, Guo-Hui He¹, Zhen-Yao Wang³, Hui-Ying Xu¹, Jin-Hua Mou^{2

4}, Zi-Hao Qin^{2

4}, Carol Sze Ki Lin², Wei-Dong Yang¹, Yalei Zhang⁵, Hong-Ye Li¹

Affiliations

¹ Key Laboratory of Eutrophication and Red Tide Prevention of Guangdong Higher Education Institutes, College of Life Science and Technology, Jinan University, Guangzhou, 510632, China.
² School of Energy and Environment, City University of Hong Kong, Tat Chee Avenue, Kowloon, Hong Kong.
³ Centre for Technology in Water and Wastewater, School of Civil and Environmental Engineering, University of Technology Sydney, Ultimo, NSW, 2007, Australia.
⁴ Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou, 510000, China.
⁵ State Key Laboratory of Pollution Control and Resources Reuse, College of Environmental Science and Engineering, Tongji University, Shanghai, 200092, China.

Abstract

When organophosphate pesticides (OPs) are not used and handled in accordance with the current rules and standards, it results in serious threats to the aquatic environment and human health. Phaeodactylum tricornutum is a prospective microalgae-based system for pollutant removal and carbon sequestration. Genetically engineered P. tricornutum, designated as the OE line (endogenously expressing purple acid phosphatase 1 [PAP1]), can utilize organic phosphorus for cellular metabolism. However, the competencies and mechanisms of the microalgae-based system (namely the OE line of P. tricornutum) for metabolizing OPs remain to be addressed. In this study, the OE line exhibited the effective biodegradation competencies of 72.12% and 68.2% for 30 mg L^-1 of dichlorvos and 50 mg L^-1 of glyphosate, accompanied by synergistic accumulations of biomass (0.91 and 0.95 g L^-1) and lipids (32.71% and 32.08%), respectively. Furthermore, the biodiesel properties of the lipids from the OE line manifested a high potential as an alternative feedstock for microalgae-based biofuel production. A plausible mechanism of OPs biodegraded by overexpressed PAP1 is that sufficient inorganic P for adenosine triphosphate and concurrent carbon flux for the reduced form of nicotinamide adenine dinucleotide phosphate biosynthesis, which improved the OP tolerance and biodegradation competencies by regulating the antioxidant system, delaying programmed cell death and accumulating lipids via the upregulation of related genes. To sum up, this study demonstrates a potential strategy using a genetically engineered strain of P. tricornutum to remove high concentrations of OPs with the simultaneous production of biomass and biofuels, which might provide novel insights for microalgae-based pollutant biodegradation.

Keywords: Biodegradation; Lipid accumulation; Organophosphate pesticide; Phaeodactylum tricornutum; Purple acid phosphatase.