Immune responses to ZnO nanoparticles are modulated by season and environmental temperature in the blue mussels Mytilus edulis

Abstract

Increased production and release of ZnO nanoparticles (nZnO) can cause toxic effects on marine ecosystems and aquatic organisms. However, nZnO toxicity and its modulation by common environmental stressors such as temperature are not yet fully understood. We examined the responses of immune cells (hemocytes) of the blue mussels (Mytilus edulis) exposed to different concentrations (0, 10, 100 μg l−1) of nZnO or dissolved zinc combined with two temperatures (ambient (10 °C in winter and 15 °C in summer) and warming (+5 °C above ambient temperature)) in winter and summer for 21 days. In winter mussels, exposure to nZnO induced a strong transcriptomic response in multiple immune and inflammation-related genes, stimulated phagocytosis and hemocyte mortality yet suppressed adhesion capacity of hemocytes. In summer mussels, the immune cell responses to nZnO were blunted. The transcriptional responses of hemocytes to dissolved Zn were qualitatively similar but weaker than the responses to nZnO. In the absence of the toxic stress, +5 °C warming lead to dysregulation of the transcription of key immune-related genes in the summer but not the winter mussels. Seasonal warm acclimatization and additional warming in summer suppressed the nZnO-induced transcriptional upregulation of antimicrobial peptides, Toll-like receptors and the complement system. These findings demonstrate that nZnO act as an immunogen in M. edulis and indicate that +5 °C warming might have detrimental effect on innate immunity of the temperate mussel populations in summer when exposure to pathogens is especially high.Capsule: ZnO nanoparticles act as an immunotoxicant inducing a strong immune response in the mussels which is dysregulated by warming in summer but not in winter.