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 profiles of key genes of the xenobiotic biotransformation system (cytochrome P450 1A [cyp1a] and glutathione S-tranferase [gst]), oxidative stress system (glutathione 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 fish bile. The results of this study revealed that fish 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.
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References
Ackerly KL, Esbaugh AJ (2020) The additive effects of oil exposure and hypoxia on aerobic performance in red drum (Sciaenops ocellatus). Sci Total Environ 737:140–174. https://doi.org/10.1016/j.scitotenv.2020.140174
Améndola-Pimenta M, Cerqueda-García D, Zamora-Briseño JA et al (2020) Toxicity evaluation and microbiota response of the lined sole Achirus lineatus (Chordata: Achiridae) exposed to the light petroleum water-accommodated fraction (WAF). J Toxicol Environ Health A 83:313–329
Anderson JW, Lee RF (2006) Use of biomarkers in oil spill risk assessment in the marine environment use of biomarkers in oil spill risk assessment in the marine environment. Hum Ecol Risk Assess 12:1192–1222. https://doi.org/10.1080/10807030600976600
Anderson CM, Mayes M, LaBelle R (2012) Update of occurrence rates for offshore oil spills. OCS Rep BOEM 69:2012–2069
Arinç E, Yilmaz D, Bozcaarmutlu A (2014) Mechanism of inhibition of CYP1A1 and glutathione S-transferase activities in fish liver by quercetin, resveratrol, naringenin, hesperidin, and rutin. Nutr Cancer. https://doi.org/10.1080/01635581.2015.965335
Beliaeff B, Burgeot T (2002) Integrated biomarker response: a useful tool for ecological risk assessment. Environ Toxicol Chem 21(6):1316–1322. https://doi.org/10.1002/etc.5620210629
Boehm PD, Cook LL, Murray KJ (2011) Aromatic hydrocarbon concentration in seawater: deepwater horizon oil spill. Int Oil Spill Conf Proc. https://doi.org/10.7901/2169-3358-2011-1-371
Brammell BF, Price DJ, Birge WJ, Elskus AA (2013) Lack of CYP1A responsiveness in species inhabiting chronically contaminated habitats: Two varieties of resistance? Comp Biochem Physiol C 157:212–219. https://doi.org/10.1016/j.cbpc.2012.07.001
Brander SM, Biales AD, Connon RE (2017) The role of epigenomics in aquatic toxicology. Environ Toxicol Chem 36:2565–2573. https://doi.org/10.1002/etc.3930
Casanova FM, Honda RT, Ferreira-nozawa MS (2013) Effects of copper and cadmium exposure on mRNA expression of catalase, glutamine synthetase, cytochrome P450 and heat shock protein 70 in tambaqui fish (Colossoma macropomum). Gene Expr Genet Genom. https://doi.org/10.4137/GGG.S10716
Cavalli G, Heard E (2019) Advances in epigenetics link genetics to the environment and disease. Nature 571:489–499. https://doi.org/10.1038/s41586-019-1411-0
Couoh-Puga ED, Vidal-Martínez VM, Ceja-Moreno V et al (2021) Histological effects of light crude oil on Sciaenops ocellatus under experimental conditions. Bull Environ Contam Toxicol. https://doi.org/10.1007/s00128-021-03172-0
Di Rienzo JA, Casanoves F, Balzarini MG, Gonzalez L, Tablada M, Robledo CW (2016) InfoStat versión 2016e. Grupo InfoStat, FCA, Universidad Nacional de Córdoba, Argentina. http://www.infostat.com.ar
dos Anjos NA, Schulze T, Brack W, Val AL, Schirmer K, Scholz S (2011) Identification and evaluation of cyp1a transcript expression in fish as molecular biomarker for petroleum contamination in tropical fresh water ecosystems. Aquat Toxicol 103:46–52. https://doi.org/10.1016/j.aquatox.2011.02.004
Ern R, Esbaugh AJ (2018) Effects of salinity and hypoxia-induced hyperventilation on oxygen consumption and cost of osmoregulation in the estuarine red drum (Sciaenops ocellatus). Comp Biochem Physiol A 222:52–59. https://doi.org/10.1016/j.cbpa.2018.04.013
FAO (2005–2018) Cultured aquatic species information programme Sciaenops ocellatus. Programa de información de especies acuáticas. Texto de Cynthia K. Faulk, A. In: Departamento de Pesca y Acuicultura de la FAO. http://www.fao.org/fishery/culturedspecies/Sciaenops_ocellatus/es. Accessed 9 Apr 2020
Garcia D, Lima D, Grunig D, Almeida E (2020) Decreased malondialdehyde levels in fish (Astyanax altiparanae) exposed to diesel: evidence of metabolism by aldehyde dehydrogenase in the liver and excretion in water. Ecotoxicol Environ Saf 190:110107. https://doi.org/10.1016/j.ecoenv.2019.110107
Gold-Bouchot G, Rubio-Pina J, Montero-Muñoz J et al (2017) Pollutants and biomarker responses in two reef fish species (Haemulon aurolineatum and Ocyurus chrysurus) in the Southern Gulf of Mexico. Mar Pollut Bull 116:249–257. https://doi.org/10.1016/j.marpolbul.2016.12.073
Head JA, Mittal K, Basu N (2014) Application of the luminometric methylation assay to ecological species: tissue quality requirements and a survey of DNA methylation levels in animals. Mol Ecol Resour 14:943–952. https://doi.org/10.1111/1755-0998.12244
Higgins LG, Hayes JD (2011) Mechanisms of induction of cytosolic and microsomal glutathione transferase (GST) genes by xenobiotics and pro-inflmmatory agents. Drug Metab Rev 43:92–137. https://doi.org/10.3109/03602532.2011.567391
Johansen JL, Esbaugh AJ (2017) Sustained impairment of respiratory function and swim performance following acute oil exposure in a coastal marine fish. Aquat Toxicol 187:82–89. https://doi.org/10.1016/j.aquatox.2017.04.002
Kerr R, Kintisch E, Stokstad E (2010) Will deepwater horizon set a new standard for catastrophe? Science 328:674–675
Khursigara AJ, Perrichon P, Martinez Bautista N, Burggren WW, Esbaugh AJ (2017) Cardiac function and survival are affected by crude oil in larval red drum, Sciaenops ocellatus. Sci Total Environ 579:797–804
Kim RO, Kim BM, Hwang DS et al (2013) Evaluation of biomarker potential of cytochrome P450 1A (CYP1A) gene in the marine medaka, Oryzias melastigma exposed to water-accommodated fractions (WAFs) of Iranian crude oil. Comp Biochem Physiol C 157:172–182. https://doi.org/10.1016/j.cbpc.2012.11.003
Lushchak VI (2011) Environmentally induced oxidative stress in aquatic animals. Aquat Toxicol 101:13–30. https://doi.org/10.1016/j.aquatox.2010.10.006
Meador J, Nahrgang J (2019) Characterizing crude oil toxicity to early-life stage fish based on a complex mixture: are we making unsupported assumptions? Environ Sci Technol 53(19):11080–11092. https://doi.org/10.1021/acs.est.9b02889
Mendelssohn IA, Andersen GL, Baltz DM, Caffey RH et al (2012) Oil impacts on coastal wetlands: implications for the Mississippi River Delta ecosystem after the Deepwater Horizon oil spill. Bioscience 62(6):562–574. https://doi.org/10.1525/bio.2012.62.6.7
Metzger DCH, Schulte PM (2016) Epigenomics in marine fishes. Mar Genom. https://doi.org/10.1016/j.margen.2016.01.004
Mirbahai L, Chipman JK (2014) Epigenetic memory of environmental organisms: a reflection of lifetime stressor exposures. Mutat Res - Genet Toxicol Environ Mutagen 764–765:10–17. https://doi.org/10.1016/j.mrgentox.2013.10.003
Pegg S, Zabbey N (2013) Oil and water: the Bodo spills and the destruction of traditional livelihood structures in the Niger Delta. Commun Dev J 48(3):391–405. https://doi.org/10.1093/cdj/bst021
Perussolo MC, Guiloski IC, Lirola JR, Fockink DH et al (2019) Integrated biomarker response index to assess toxic effects of environmentally relevant concentrations of paracetamol in a neotropical catfish (Rhamdia quelen). Ecotox Environ Safe 182:109438
Peterson CH, Rice SD, Short JW, Esler D et al (2003) Long-term ecosystem response to the Exxon Valdez oil spill. Science 302:2082–2086
Puch-Hau C, Quintanilla-Mena M, Rivas-Reyes I, Patiño-Suárez V et al (2018) Clonación molecular de genes biomarcadores de contaminación en Peces que Habitan el Golfo de México. Revista del Centro de Graduados e Investigación. Instituto Tecnológico de Mérida 33(73):210–214
Puch-Hau C, Sánchez-Tapia IA, Patiño-Suárez V, Olvera-Novoa MA et al (2019) Evaluation of two independent protocols for the extraction of DNA and RNA from different tissues of sea cucumber Isostichopus badionotus. MethodsX 6:1627–1634. https://doi.org/10.1016/j.mex.2019.07.010
Pulster EL, Gracia A, Armenteros M et al (2020) A first comprehensive baseline of hydrocarbon pollution in Gulf of Mexico Fishes. Sci Rep 10:6437. https://doi.org/10.1038/s41598-020-62944-6
Quintanilla-Mena MA, Gonzalez-Garza BI, Perez-Menendez AI, Zapata-Perez O (2018) Principios epigenéticos en un contexto ecotoxicológico: niveles de metilación global en adn de peces lenguados (familia: paralichthyidae) procedentes del sur del golfo de México. En: Contribuciones al conocimiento de la Ecotoxicología y Química Ambiental en México, vol 2, 1a ed. Instituto Politécnico Nacional, pp 123–146
Quintanilla-Mena MA, Gold-Bouchot G, Zapata-Pérez O, Rubio-Piña J et al (2020) Biological responses of shoal flounder (Syacium gunteri) to toxic environmental pollutants from the southern Gulf of Mexico. Environ Pollut 258:113669. https://doi.org/10.1016/j.envpol.2019.113669
Rooker JR, Kitchens LL, Dance MA, Wells RJD, Falterman B, Cornic M (2013) Spatial, temporal, and habitat-related variation in abundance of pelagic fishes in the Gulf of Mexico: potential implications of the Deepwater Horizon oil spill. PLoS ONE 8:e76080. https://doi.org/10.1371/journal.pone.0076080.s006
Rosales M, Castillo S, Pohlenz C, Gatlin DM (2017) Evaluation of dried yeast and threonine fermentation biomass as partial fish meal replacements in the diet of red drum Sciaenops ocellatus. Anim Feed Sci Technol 232:190–197. https://doi.org/10.1016/j.anifeedsci.2017.08.014
Sanchez W, Burgeot T, Porcher JM (2013) A novel “Integrated biomarker response” calculation based on reference deviation concept. Environ Sci Pollut Res 20:2721–2725. https://doi.org/10.1007/s11356-012-1359-1
Serafin J, Guffey SC, Bosker T, Griffitt RJ, De Guise S, Perkins C et al (2019) Combined effects of salinity, temperature, hypoxia, and Deepwater Horizon oil on Fundulus grandis larvae. Ecotoxicol Environ Saf 181:106–113. https://doi.org/10.1016/j.ecoenv.2019.05.059
Turja R, Sanni S, Stankevičiūtė M, Butrimavičienė L et al (2020) Biomarker responses and accumulation of polycyclic aromatic hydrocarbons in Mytilus trossulus and Gammarus oceanicus during exposure to crude oil. Environ Sci Pollut Res 27:15498–15514. https://doi.org/10.1007/s11356-020-07946-7
Wade TL, Sericano JL, Sweet ST, Knap AH, Guinasso NL (2015) Spatial and temporal distribution of water column total polycyclic aromatic hydrocarbons (PAH) and total petroleum hydrocarbons (TPH) from the Deepwater Horizon (Macondo) incident. Mar Pollut Bull. https://doi.org/10.1016/j.marpolbul.2015.12.002
Xu EG, Khursigara AJ, Magnuson J, Hazard ES et al (2017) Larval red drum (Sciaenops ocellatus) sublethal exposure to weathered Deepwater Horizon crude oil: developmental and transcriptomic consequences. Environ Sci Technol 51:10162–10172. https://doi.org/10.1021/acs.est.7b02037
Xu EG, Khursigara AJ, Li S, Esbaugh AJ et al (2019) mRNA-miRNA- seqreveals neuro-cardio mechanisms of crude oil toxicity in red drum (Sciaenops ocellatus). Environ Sci Technol 53(6):3296–3305. https://doi.org/10.1021/acs.est.9b00150
Yoskowitz DW (2009) The productive value of the gulf of Mexico. In: Cato J (ed) Gulf of Mexico origins, waters, and biota: ocean and coastal economy. TAMU Press, College Station
Acknowledgements
We thank the staff of the Patología Acuática, Inmunologia y Biología Molecular and Geoquímica Marina laboratory of CINVESTAV, Mérida, for technical assistance and sample handling. We also thank to Dra. Abril Rodríguez-González, Danilú Couoh Puga, Clara Vivas Rodríguez, Gregory Arjona Torres and Víctor Ceja Moreno for technical assistance.
Funding
This research has been funded by the Mexican National Council for Science and Technology—Mexican Ministry of Energy—Hydrocarbon Fund, project 201441. This is a contribution of the Gulf of Mexico Research Consortium (CIGoM). We acknowledge PEMEX’s specific request to the Hydrocarbon Fund to address the environmental effects of oil spills in the Gulf of Mexico.
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This study was conducted in accordance with the Guidelines for Care and Manipulation of Laboratory Animals (PICUAL-CINVESTAV, 2002), the Mexican Official Norm (de Aluja, 2002, NOM-062-ZOO-1999), and the Guide for the Care and Use of Laboratory Animals used by the US National Institute of Health (http://www.aaalac.org/resources/Guide_2011.pdf).
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Cañizares-Martínez, M.A., Quintanilla-Mena, M., Del-Río-García, M. et al. Acute Exposure to Crude Oil Induces Epigenetic, Transcriptional and Metabolic Changes in Juvenile Sciaenops ocellatus. Bull Environ Contam Toxicol 108, 85–92 (2022). https://doi.org/10.1007/s00128-021-03241-4
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DOI: https://doi.org/10.1007/s00128-021-03241-4