Time- and Oil-Dependent Transcriptomic and Physiological Responses to Deepwater Horizon Oil in Mahi-Mahi (Coryphaena hippurus) Embryos and Larvae

Abstract

The Deepwater Horizon (DWH) oil spill contaminated the spawning habitats for numerous commercially and ecologically important fishes. Exposure to the water accommodated fraction (WAF) of oil from the spill has been shown to cause cardiac toxicity during early developmental stages across fishes. To better understand the molecular events and explore new pathways responsible for toxicity, RNA sequencing was performed in conjunction with physiological and morphological assessments to analyze the time-course (24, 48, and 96 h post fertilization (hpf)) of transcriptional and developmental responses in embryos/larvae of mahi-mahi exposed to WAF of weathered (slick) and source DWH oils. Slick oil exposure induced more pronounced changes in gene expression over time than source oil exposure. Predominant transcriptomic responses included alteration of EIF2 signaling, steroid biosynthesis, ribosome biogenesis and activation of the cytochrome P450 pathway. At 96 hpf, slick oil exposure resulted in significant perturbations in eye development and peripheral nervous system, suggesting novel targets in addition to the heart may be involved in the developmental toxicity of DHW oil. Comparisons of changes of cardiac genes with phenotypic responses were consistent with reduced heart rate and increased pericardial edema in larvae exposed to slick oil but not source oil.

Novel transcriptome assembly and comparative toxicity pathway analysis in mahi-mahi (Coryphaena hippurus) embryos and larvae exposed to Deepwater Horizon oil

“…Methylsterol monooxygenase 1 ( msmo1 ), functions in cholesterol biosynthesis, exemplified another top upregulated gene (4.4 fold by both de novo and OnRamp approaches). The expression patterns of nine selected genes in 96 hpf larvae after slick oil exposure were verified by RT-qPCR (quantitative real-time PCR)10.…”

“…In contrast, our previous study used a commercially available reference-transcriptome-guided automated OnRamp approach that failed to provide sequence information for de novo transcriptome assembly efforts for mahi-mahi10. To confirm prior molecular signatures and provide an accessible transcriptome data base, differential expression analysis was conducted in 96 hpf larvae exposed to slick oil by the de novo approach, and downstream gene ontology (GO) terms were compared to the 24, 48 and 96 hpf mahi-mahi exposed to both source and slick oil as determined by the earlier OnRamp approach.…”

“…The DHW oil is a complex chemical mixture, with polycyclic aromatic hydrocarbons (PAHs) and their alkylated homologues being the main toxic components to fish embryos78. The composition and structure of individual PAHs in the water column can be significantly altered by weathering processes, and it has been shown that weathered surface slick oil (3- and 4-ring PAHs enriched) is more toxic than non-weathered source oil to mahi-mahi on a ∑PAH basis at different levels from molecular to physiological functions910. Numerous studies have investigated the developmental toxicity of crude oil to fish embryos and larvae and identified a variety of abnormalities such as cardiac function, kidney development, formation of the craniofacial skeleton (eye and jaw), nervous system as well as reduced swimming performance710111213.…”

“…The composition and structure of individual PAHs in the water column can be significantly altered by weathering processes, and it has been shown that weathered surface slick oil (3- and 4-ring PAHs enriched) is more toxic than non-weathered source oil to mahi-mahi on a ∑PAH basis at different levels from molecular to physiological functions910. Numerous studies have investigated the developmental toxicity of crude oil to fish embryos and larvae and identified a variety of abnormalities such as cardiac function, kidney development, formation of the craniofacial skeleton (eye and jaw), nervous system as well as reduced swimming performance710111213. These impacted functions and biological processes may contribute to delayed mortality and declined population as previously observed in pink salmon ( Oncorhynchus gorbuscha ) exposed to crude oil1415.…”

“…Another study in mahi-mahi focused on the developmental cardiotoxicity of crude oil exposure targeted ten molecular indicators of cardiac stress and injury, such as atrial and ventricular myosin heavy chains ( amhc / myh6 and vhmc / myh7 ), cardiac myosin light chain 2 ( cmlc2 / myl7 ), B-type natriuretic peptide ( nppb ), as well as transcription factors nkx2.5 and tbx5 17. Our previous study by RNA sequencing and physiological assessment demonstrated that slick oil exposure resulted in pronounced perturbations in metabolism, steroid biosynthesis, vision, and AhR genes suggesting other targets in addition to the heart may be involved in the developmental toxicity of DHW oil10. Given the increasing evidence of morphological and physiological impacts of crude oil on a number of fish species, a comprehensive and accessible genomic database is urgently needed for target species in oiled regions to advance our understanding of the toxic molecular mechanisms of crude oil.…”