Genome-Wide Molecular Adaptation in Algal Primary Productivity Induced by Prolonged Exposure to Environmentally Realistic Concentration of Nanoplastics

Little information is known about the long-term effects of nanoplastics (NPs) in aquatic environments, especially under environmental-related scenarios. Herein, three differently charged NPs (nPS, nPS-NH₂, and nPS-COOH) were exposed at an environmentally realistic concentration (10 μg/L) for 100 days to explore the variation of primary productivity (i.e., algae) in aquatic ecosystems. Our results demonstrated that the algae adapted to all three types of NPs by enhancing the algal number (by 10.34–16.52%), chlorophyll a (by 11.28–17.65%), and carbon-fixing enzyme activity (by 49.19–68.33%), which were further confirmed by the exposure results from natural water culturing experiments. Based on the algal chloroplast number and biovolume at the individual level, only nPS caused algal differentiation into two heterogeneous subpopulations (54.92 vs 45.08%), while nPS-NH₂ and nPS-COOH did not cause the differentiation of the algal population. Moreover, the molecular adaptation mechanisms of algae to NPs were unraveled by integrating epigenomics and transcriptomics. Mean methylation rates of algae on exposure to nPS, nPS-NH₂, and nPS-COOH were significantly elevated. In addition, the direction of gene expression regulation via differentially methylated regions associated with genes when exposed to nPS-COOH was distinct from those of nPS and nPS-NH₂. Our results highlight the importance of assessing the long-term ecotoxicity of NPs and provide useful information for understanding the effect of NPs on aquatic ecosystems.