Route-dependent toxicodynamics of 6PPD-quinone in mussels: Mechanical resilience trades off with subcellular injury and metabolic disruption

Abstract

The byssal thread, a mussel-secreted proteinaceous anchor critical for underwater adhesion, represents a vital adaptation for survival in dynamic marine environments but faces vulnerability to pollutants. This study examines how the tire-derived contaminant 6PPD-quinone (6PPD-Q) impacts the byssal defense system of Mytilus coruscus via waterborne and dietary exposure. Experiments evaluated byssal production, mechanical traits, foot histology, and transcriptomic profiles. Waterborne 6PPD-Q induced a paradoxical enhancement: increased thread count/diameter and adhesion strength coexisted with progressive foot tissue damage, evidenced by histopathology and dysregulated ribosomal/DNA repair pathways. Dietary exposure, conversely, disrupted nutrient metabolism and immune responses, with transcriptomes diverging sharply from waterborne cases. KEGG analysis revealed route-specific toxicity: waterborne exposure activated nuclear DNA damage pathways, while dietary exposure triggered lysosomal/antigen-processing mechanisms. Solvent controls confirmed 6PPD-Q specificity. These findings unveil a dual paradox where 6PPD-Q simultaneously enhances mechanical resilience and inflicts subcellular harm, with toxicodynamics governed by exposure route. The trade-off between structural fortification and physiological impairment highlights complex pollutant interactions in mussels, emphasizing the need for exposure pathway-specific assessments in managing aquaculture sustainability amid coastal contamination. This work advances understanding of anthropogenic pollutant impacts on marine bivalve adaptive strategies and ecosystem health.