Vol.:(0123456789) 1 3 Bulletin of Environmental Contamination and Toxicology https://doi.org/10.1007/s00128-021-03241-4 Acute Exposure to Crude Oil Induces Epigenetic, Transcriptional and Metabolic Changes in Juvenile Sciaenops ocellatus Mayra A. Cañizares‑Martínez 1  · Mercedes Quintanilla‑Mena 1  · Marcela Del‑Río‑García 1  · Isajav Rivas‑Reyes 1  · María V. Patiño‑Suárez 1  · Victor M. Vidal‑Martínez 1  · M. Leopoldina Aguirre‑Macedo 1  · Carlos A. Puch‑Hau 1 Received: 5 June 2020 / Accepted: 17 April 2021 © The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature 2021 Abstract In this study, we report molecular and metabolic responses of Sciaenops ocellatus during an acute oil exposure bioassay (100, 800 and 8000 mg 1 –1 of crude oil). The global DNA methylation and expression profles of key genes of the xenobiotic biotransformation system (cytochrome P450 1A [cyp1a] and glutathione S-tranferase [gst]), oxidative stress system (glu- tathione peroxidase [gpx], catalase [cat], aldehyde dehydrogenase [aldh]) and reproductive system (vitellogenin [vtg]) were evaluated. At the metabolic level, we evaluated the concentration of four polycyclic aromatic hydrocarbon (PAH) metabolites -hydroxybenzo[a]pyrene, hydroxypyrene, hydroxynaphthalene and hydroxyphenanthrene- in fsh bile. The results of this study revealed that fsh exposed to crude oil exhibited hypomethylation of DNA, up-regulation of cyp1a and gst and down- regulation of gpx, cat, aldh and vtg and high concentrations of PAH metabolites with respect to the control. Keywords Red drum · Hydrocarbon · PAH metabolites · DNA methylation · Gene expression The Gulf of Mexico (GoM) produces 124.01 billion USD for Mexico and the United States on a yearly basis (Yoskow- itz 2009). One of the main economic activities that con- tribute to this afuence is the exploration and extraction of oil. Unfortunately, this endeavor has caused more than 340 large marine oil spills (Anderson et al. 2012). Well known examples of the high risk involved in oil extraction activi- ties are the Exxon Valdez oil spill (Peterson et al. 2003), the Deepwater Horizon (DWH) disaster (Kerr et al. 2010) and most recently, the 2016 Royal Dutch Shell incident (Pegg and Zabbey 2013). Among marine organisms, fsh stocks may be especially vulnerable to oil spills (Rooker et al. 2013). The specifc efects on these organisms can be very complex and dif- fcult to predict in the environment. For this reason, toxicity bioassays represent an important tool to evaluate specifc responses. Based on these responses, it is possible to infer whether those efects observed in fsh naturally exposed to environmental pollutants are associated with the specifc agents of interest such as hydrocarbons (Anderson and Lee 2006). Epigenetic analysis has been an important tool to evalu- ate the interaction between pollutants and individual marine organisms (Brander et al. 2017). One well-known epige- netic mechanism is DNA methylation, defned as a methyl group added to cytosine nucleotides by DNA methyltrans- ferases. Changes in global DNA methylation levels (specif- cally hypomethylation: low methylation levels) have been observed as a response to toxic compounds (Quintanilla- Mena et al. 2020). This phenomenon alters the transcription of genes involved in early development, metabolism, repro- duction and oncogenesis and resulting in the generation of several diseases, such as reproductive impairment and cancer (Brander et al. 2017). At the transcript level, pollutants can induce dysregula- tion of a battery of genes involved in cell detoxifcation (CD), oxidative stress (OS) and reproductive systems. The PAH contained in crude oil can cause an overexpression of CD system genes (cytochrome P450 1A [cyp1a] and glutathione S-transferase [gst]), resulting in the generation of PAH metabolites that are excreted through the bile (dos Anjos et al. 2011; Higgins and Hayes 2011). Although this mechanism contributes to the detoxifcation of cells during * Carlos A. Puch-Hau Carlos.Puch@cinvestav.mx; cashi026@hotmail.com 1 Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, Departamento de Recursos del Mar, Unidad Mérida, Km. 6 Antigua Carretera a Progreso, Cordemex, 97310 Mérida, Yucatán, Mexico