Toxicity of microplastics and nano-plastics to coral-symbiotic alga (Dinophyceae Symbiodinium): Evidence from alga physiology, ultrastructure, OJIP kinetics and multi-omics

Shiqi Jiang; Huiting Lu; Yingyin Xie; Tingrui Zhou; Zhenqing Dai; Ruikun Sun; Lei He; Chengyong Li

doi:10.1016/j.watres.2024.123002

Toxicity of microplastics and nano-plastics to coral-symbiotic alga (Dinophyceae Symbiodinium): Evidence from alga physiology, ultrastructure, OJIP kinetics and multi-omics

Water Res. 2024 Dec 17:273:123002. doi: 10.1016/j.watres.2024.123002. Online ahead of print.

Authors

Shiqi Jiang¹, Huiting Lu¹, Yingyin Xie¹, Tingrui Zhou¹, Zhenqing Dai², Ruikun Sun², Lei He³, Chengyong Li⁴

Affiliations

¹ School of Chemistry and Environment, Guangdong Ocean University, Zhanjiang, 524088, China.
² School of Chemistry and Environment, Guangdong Ocean University, Zhanjiang, 524088, China; Analytical and Testing Center for Ocean in Western of Guangdong Province, Guangdong Provincial Observation and Research Station for Tropical Ocean Environment in Western Coastal Water, Guangdong Ocean University, Zhanjiang, 524088, China.
³ Analyzing and Testing Center, Guangdong Ocean University, Zhanjiang, 524088, China. Electronic address: [email protected].
⁴ School of Chemistry and Environment, Guangdong Ocean University, Zhanjiang, 524088, China; Analyzing and Testing Center, Guangdong Ocean University, Zhanjiang, 524088, China; Analytical and Testing Center for Ocean in Western of Guangdong Province, Guangdong Provincial Observation and Research Station for Tropical Ocean Environment in Western Coastal Water, Guangdong Ocean University, Zhanjiang, 524088, China. Electronic address: [email protected].

PMID: 39709880
DOI: 10.1016/j.watres.2024.123002

Abstract

Corals are representative of typical symbiotic organisms. The coral-algal (Symbiodinium spp.) symbiosis drives the productivity of entire coral reefs. In recent years, microplastics (MPs) and nano-plastics (NPs) have been shown to disrupt this symbiosis, leading to coral bleaching. However, how MPs/NPs affect the Symbiodinium spp. is less thoroughly explored. In this work, Dinophyceae Symbiodinium was employed as a model to study the toxicity effects of MPs and NPs with different concentrations (covering environment-related concentration) toward algae in terms of cellular responses, ultrastructure, OJIP kinetics curve and multi-omics. MPs and NPs caused adverse effects on algae growth throughout whole growing phase, with only slight differences observed in the maximal inhibition ratio. In addition to cell surface shrinkage, holes and plate sutures shedding of algae, the presence of distorted thylakoids, plasmolysis and expanded vesicle volume were observed due to the oxidative stress and physical damage caused by MPs/NPs. The results of OJIP kinetics and JIP-test revealed that MPs/NPs-induced deactivation of oxygen-releasing complex (OEC) centers, reduced electron transfer (photosystem II, PSII), and inefficient energy conversion of antenna proteins were the primary factors for photosynthesis reduction. Weighted correlation network analysis (WGCNA) showed that the impairment of photosynthesis further induces metabolic disturbances, including reactive oxygen species (ROS) generation and nucleotide metabolism dysregulation, thereby exacerbating DNA damage in the algae. Proteomics further validate the accuracy of our results and underscore the significance of the phosphatidylinositol (PI) signaling system in algae responding to MP/NPs acclimation. Collectively, our findings provide comprehensive insights into the ecotoxicity of NPs/MPs on symbiotic algae.

Keywords: Dinophyceae Symbiodinium; Microplastics; Multi-omics; Nano-plastics; Ultrastructure.