Exploring cell aggregation as a defense strategy against perchlorate stress in Chlamydomonas reinhardtii through multi-omics analysis

Xianyuan Zhang; Yixiao Zhang; Zixu Chen; Peifan Gu; Xiaoyan Li; Gaohong Wang

doi:10.1016/j.scitotenv.2023.167045

Exploring cell aggregation as a defense strategy against perchlorate stress in Chlamydomonas reinhardtii through multi-omics analysis

Sci Total Environ. 2023 Dec 20:905:167045. doi: 10.1016/j.scitotenv.2023.167045. Epub 2023 Sep 12.

Authors

Xianyuan Zhang¹, Yixiao Zhang², Zixu Chen¹, Peifan Gu¹, Xiaoyan Li³, Gaohong Wang⁴

Affiliations

¹ Key Laboratory for Algae Biology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China; University of Chinese Academy of Sciences, Beijing 100049, China.
² Key Laboratory for Algae Biology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China; School of Science, Tibet University, Lasha 850000, China.
³ Key Laboratory for Algae Biology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China. Electronic address: lixiaoyan@ihb.ac.cn.
⁴ Key Laboratory for Algae Biology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China; University of Chinese Academy of Sciences, Beijing 100049, China. Electronic address: space@ihb.ac.cn.

PMID: 37709088
DOI: 10.1016/j.scitotenv.2023.167045

Abstract

Perchlorate (ClO₄^-) is a type of novel, widely distributed, and persistent inorganic pollutant. However, the impacts of perchlorate on freshwater algae remain unclear. In this study, the response and defense mechanisms of microalgae (Chlamydomonas reinhardtii) under perchlorate stress were investigated by integrating physiological and biochemical monitoring, transcriptomics, and metabolomics. Weighted gene co-expression network analysis (WGCNA) of transcriptome data was used to analyze the relationship between genes and phenotype and screen the key pathways. C. reinhardtii exhibited aggregate behavior when exposed to 100- and 200-mM perchlorate but was restored to its unicellular lifestyle when transferred to fresh medium. WGCNA results found that the "carbohydrate metabolism" and "lipid metabolism" pathways were closely related to cell aggregation phenotype. The differential expression genes (DEGs) and differentially accumulated metabolites (DAMs) of these pathways were upregulated, indicating that the lipid and carbohydrate metabolisms were enhanced in aggregated cells. Additionally, most genes and metabolites related to phytohormone abscisic acid (ABA) biosynthesis and the mitogen-activated protein kinase (MAPK) signaling pathway were significantly upregulated, indicating their crucial roles in the signal transmission of aggregated cells. Meanwhile, in aggregated cells, extracellular polymeric substances (EPS) and lipid contents increased, photosynthesis activity decreased, and the antioxidant system was activated. These characteristics contributed to C. reinhardtii's improved resistance to perchlorate stress. Above results demonstrated that cell aggregation behavior was the principal defense strategy of C. reinhardtii against perchlorate. Overall, this study sheds new light on the impact mechanisms of perchlorate to aquatic microalgae and provides multi-omics insights into the research of multicellular-like aggregation as an adaptation strategy to abiotic stress. These results are beneficial for assessing the risk of perchlorate in aquatic environments.

Keywords: C. reinhardtii; Cell aggregation; Defense strategy; Multi-omics analysis; Perchlorate.

MeSH terms

Chlamydomonas reinhardtii* / physiology
Lipids
Multiomics
Perchlorates / metabolism
Perchlorates / toxicity

Substances

perchlorate
Perchlorates
Lipids