Reactive oxygen species derived from NADPH oxidase as signaling molecules regulate fatty acids and astaxanthin accumulation in Chromochloris zofingiensis

Yi Yuan; Tiantian Zhao; Weizheng Gao; Wenqi Ye; Yuling Chen; Dongzhe Sun; Zhao Zhang

doi:10.3389/fmicb.2024.1387222

Reactive oxygen species derived from NADPH oxidase as signaling molecules regulate fatty acids and astaxanthin accumulation in Chromochloris zofingiensis

Front Microbiol. 2024 Apr 29:15:1387222. doi: 10.3389/fmicb.2024.1387222. eCollection 2024.

Authors

Yi Yuan^#¹, Tiantian Zhao^#¹, Weizheng Gao², Wenqi Ye², Yuling Chen¹, Dongzhe Sun¹, Zhao Zhang¹

Affiliations

¹ Ministry of Education Key Laboratory of Molecular and Cellular Biology, Hebei Collaborative Innovation Center for Eco-Environment, Hebei Research Center of the Basic Discipline of Cell Biology, College of Life Sciences, Hebei Normal University, Shijiazhuang, China.
² School of Life Sciences, Hebei University, Baoding, China.

^# Contributed equally.

Abstract

Abiotic stresses can increase the total fatty acid (TFA) and astaxanthin accumulation in microalgae. However, it remains unknown whether a unified signal transduction mechanism exists under different stresses. This study explored the link between nicotinamide adenine dinucleotide phosphate (NADPH) oxidase-derived reactive oxygen species (ROS) and the accumulation of fatty acids and astaxanthin in Chromochloris zofingiensis under three abiotic stresses. Results showed significant increases in fatty acid, astaxanthin, and ROS levels under nitrogen deficiency, phosphorus deficiency, and high-salinity stress. The introduction of the NADPH oxidase inhibitor diphenyleneiodonium (DPI) decreased the content of these components. This underscores the pivotal role of NADPH oxidase-derived ROS in the accumulation of fatty acid and astaxanthin under abiotic stress. Analysis of transcriptomes across three conditions following DPI addition revealed 1,445 shared differentially expressed genes (DEGs). Enrichment analysis revealed that biotin, betalain, thiamine, and glucosinolate may be important in stress responses. The heatmap demonstrated that DPI notably suppressed gene expression in the fatty acid and carotenoid biosynthesis pathways. Our findings underscore the pivotal role of NADPH oxidase-derived ROS in the accumulation of fatty acid and astaxanthin under abiotic stresses.

Keywords: Chromochloris zofingiensis; NADPH oxidase; ROS; WGCNA analysis; astaxanthin; fatty acid; transcriptomic analysis.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This study was financially supported by the National Natural Science Foundation of China (Project No. 32101925), Science Foundation of Hebei Normal University (Project Nos. L2023B20 and L2024B22), and Post-graduate’s Innovation Fund Project of Hebei University (HBU2023SS016).