Abstract
Salmon exposed to waterborne metals can experience olfactory impairment leading to disrupted chemosensation. In the current study, we investigated the effects of cadmium (Cd) on salmon olfactory function by modeling an exposure scenario where juvenile salmon transiently migrate through a polluted waterway. Coho were exposed to environmentally relevant concentrations of waterborne Cd (2 and 30 µg/L) for 48 h and (0.3 and 2 μg/L) for 16 days, followed by a 16-day depuration associated with outmigration. Cadmium exposures inhibited behavioral responses towards L-cysteine and conspecific odorants, with effects persisting following the depuration. Behavioral alterations following the 30 µg/L exposure were associated with increased olfactory epithelial gene expression of metallothionein (mt1a) and heme oxygenase (hmox1); reduced expression of olfactory signal transduction (OST) molecules; and reduced expression of mRNAs encoding major coho odorant receptors (ORs). Salmon OR array analysis indicated that Cd preferentially impacted expression of OST and OR markers for ciliated olfactory sensory neurons (OSNs) relative to microvillus OSNs, suggesting a differential sensitivity of these two major OSN populations. Behavioral alterations on exposure to 0.3 and 2 µg/L Cd were associated with increased mt1a, but not with major histological or OR molecular changes, likely indicating disrupted OST as a major mechanism underlying the behavioral dysfunction at the low-level Cd exposures. Laser-ablation mass spectrometry analysis revealed that the OSN injury and behavioral dysfunction was associated with significant Cd bioaccumulation within the olfactory sensory epithelium. In summary, low-level Cd exposures associated with polluted waterways can induce differential and persistent olfactory dysfunction in juvenile coho salmon.