Macondo crude oil from the Deepwater Horizon oil spill disrupts specific developmental processes during zebrafish embryogenesis

Abstract

BackgroundThe Deepwater Horizon disaster was the largest marine oil spill in history, and total vertical exposure of oil to the water column suggests it could impact an enormous diversity of ecosystems. The most vulnerable organisms are those encountering these pollutants during their early life stages. Water-soluble components of crude oil and specific polycyclic aromatic hydrocarbons have been shown to cause defects in cardiovascular and craniofacial development in a variety of teleost species, but the developmental origins of these defects have yet to be determined. We have adopted zebrafish, Danio rerio, as a model to test whether water accumulated fractions (WAF) of the Deepwater Horizon oil could impact specific embryonic developmental processes. While not a native species to the Gulf waters, the developmental biology of zebrafish has been well characterized and makes it a powerful model system to reveal the cellular and molecular mechanisms behind Macondo crude toxicity.ResultsWAF of Macondo crude oil sampled during the oil spill was used to treat zebrafish throughout embryonic and larval development. Our results indicate that the Macondo crude oil causes a variety of significant defects in zebrafish embryogenesis, but these defects have specific developmental origins. WAF treatments caused defects in craniofacial development and circulatory function similar to previous reports, but we extend these results to show they are likely derived from an earlier defect in neural crest cell development. Moreover, we demonstrate that exposure to WAFs causes a variety of novel deformations in specific developmental processes, including programmed cell death, locomotor behavior, sensory and motor axon pathfinding, somitogenesis and muscle patterning. Interestingly, the severity of cell death and muscle phenotypes decreased over several months of repeated analysis, which was correlated with a rapid drop-off in the aromatic and alkane hydrocarbon components of the oil.ConclusionsWhether these teratogenic effects are unique to the oil from the Deepwater Horizon oil spill or generalizable for most crude oil types remains to be determined. This work establishes a model for further investigation into the molecular mechanisms behind crude oil mediated deformations. In addition, due to the high conservation of genetic and cellular processes between zebrafish and other vertebrates, our work also provides a platform for more focused assessment of the impact that the Deepwater Horizon oil spill has had on the early life stages of native fish species in the Gulf of Mexico and the Atlantic Ocean.

Deepwater Horizon crude oil impacts the developing hearts of large predatory pelagic fish

“…The above crude oil cardiotoxicity syndrome has been extensively characterized in zebrafish embryos exposed to several geologically distinct oils (17,21,23,30,31), including the Mississippi Canyon 252 (MC252) crude oil released from the blown out Deepwater Horizon wellhead (20,32). Similar effects have been reported for temperate marine and anadromous species, such as Pacific herring (19,26,27,33) and pink salmon (34,35), following exposure to Alaska North Slope crude oil.…”

Low reproductive success rates of common bottlenose dolphins Tursiops truncatus in the northern Gulf of Mexico following the Deepwater Horizon disaster (2010-2015)

“…In seabird colonies, successful annual reproduction was still 70% lower than historical rates, 5 yr after the Prestige oil spill (Barros et al 2014). Reproductive and early developmental effects have also been documented in fish species exposed to oil from the Exxon Valdez, Prestige, and Deep water Horizon spills (Hawkes & Stehr 1982, Kocan et al 1996, Bilbao et al 2010, de Soysa et al 2012, Kawa guchi et al 2012, Whitehead et al 2012, Turner et al 2014.…”

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“…The results indicated that WAF 10W-40 motor oil affected the early life stage embryos of zebrafish a dose-dependent manner. Embryotoxic effects such as weak pigmentation, tail defects, and reduced heartbeat rate were reported in embryos exposed to 15, 33 and 50 v/v crude oil during 96 h (Pauka et al, 2011). De Soysa et al (2012 indicated that the Maconda crude oil WAF caused a various defects in zebrafish embryos.…”