mRNA-miRNA-Seq Reveals Neuro-Cardio Mechanisms of Crude Oil Toxicity in Red Drum (Sciaenops ocellatus)

Polycyclic aromatic hydrocarbons (PAHs) present in crude oil can cause global gene dysregulation and developmental impairment in fish. However, the mechanisms that alter gene regulation are not well understood. In this study, larval red drum (Sciaenops ocellatus) were exposed to water accommodated fractions of source oil (6.8, 13.7, and 35.9 μg/L total PAHs) and weathered slick oil (4.7, 8.1, and 18.0 μg/L total PAHs) from the Deepwater Horizon (DWH) oil spill. The global mRNA-microRNA functional networks associated with the toxicity of DWH oil were explored by next-generation sequencing and in-depth bioinformatics analyses. Both source and slick oil significantly altered the expression of miR-18a, miR-27b, and miR-203a across all exposure concentrations. Consistent with the observed concentration-dependent morphological changes, the target mRNAs of these microRNAs were predominantly involved in neuro-cardio system development processes and associated key signaling pathways such as axonal guidance signaling, cAMP-response-element-binding protein signaling in neurons, calcium signaling, and nuclear-factor-of-activated T cells signaling in cardiac hypertrophy. The results indicated that the developmental toxicity of crude oil may result from the abnormal expression of microRNAs and associated target genes, especially for the nervous system. Moreover, we provide a case study for systematic toxicity evaluation leveraging mRNA-microRNA-seq data using nonmodel species.