The rapid proliferation of lithium-ion battery technologies has intensified lithium (Li) discharge into coastal aquatic environments, raising growing concerns about its ecological risks as an emerging pollutant. Akashiwo sanguinea, a dinoflagellate responsible for recurring harmful algal blooms (HABs) in the South China Sea, represents a particularly relevant yet understudied model organism for assessing the ecotoxicological impacts of dissolved lithium on marine primary producers. This study investigated the physiological, transcriptomic, and metabolomic responses of A. sanguinea to dissolved lithium chloride (LiCl) across environmentally relevant and elevated concentrations (0, 1, and 100 mg/L) over a 14-day exposure period.

Physiological assessments revealed concentration-dependent but divergent responses. At the environmentally relevant concentration (1 mg/L), A. sanguinea exhibited a hormetic response, characterized by stimulated cell proliferation alongside elevated oxidative stress markers and reduced chlorophyll content. In contrast, exposure to 100 mg/L LiCl resulted in severe growth inhibition, the highest levels of superoxide dismutase (SOD) and catalase (CAT) activity, maximal malondialdehyde (MDA) accumulation, and the lowest chlorophyll levels across all treatments — collectively indicating pronounced lipid peroxidation and oxidative damage.

To elucidate the underlying molecular mechanisms, integrated transcriptomic and metabolomic analyses were conducted on samples collected at day 8, coinciding with the transition from the exponential to the stationary growth phase. Transcriptomic profiling identified significant differential expression in genes associated with photosynthesis, oxidative stress response, and cell membrane integrity. Concurrent metabolomic analysis revealed marked perturbations in pathways governing energy metabolism and amino acid biosynthesis. Cross-omics integration suggests that dissolved lithium disrupts the photosynthetic electron transport chain, triggering reactive oxygen species (ROS) overproduction that cascades into broad metabolic dysregulation and compromised cellular structural integrity.

This study provides mechanistic insights into the toxicity of dissolved lithium in a HAB-forming dinoflagellate, and importantly, documents a hormetic effect at environmentally realistic Li concentrations. These findings establish critical baseline data for the ecological risk assessment of lithium as an emerging new energy pollutant in coastal marine systems.