Macondo crude oil from the Deepwater Horizon oil spill disrupts specific developmental processes during zebrafish embryogenesis (teratogen!)

[Emily]

Figure 1. Exposure to Macondo crude oil-derived WAFs induced diverse gross morphological deformations in zebrafish embryos. (A-F) Lateral and ventral views of live untreated control (A, B) and WAF-treated embryos (C-F) at 5 dpf. Severe cardiac and yolk edema (C, D, E, arrows), dorsal tail curvature (E, F, double arrows), and cysts at the tip of the tail (C, D, F, arrowhead) were visible. (G, H) WAF-treated embryos (H) had reduced jaws compared to controls (G, brackets). (G-J) At 3 dpf cardiac edema was evident in WAF-treated embryos (arrows), and 28% of embryos had hemorrhaging in the forebrain, midbrain and hindbrain (arrowheads). Lateral (G, H, I, J) and dorsal views (H', I', J'). (K-M) Retinal architecture appeared normal in control and WAF-treated embryos (K, L) but there was a slight reduction in the area and perimeter of WAF-treated retinas (M). Except for lens area, the size reductions were statistically significant (M, asterisks; t-tests: lens area, P = 0.015; lens perimeter, P = 0.007; retina area P < 0.0005; retina perimeter, P < 0.0005). Scale bars: 200 μm, F, J'; 50 μm, L. Abbreviations: gcl, ganglion cell layer; ipl, inner plexiform layer; inl, inner nuclear layer; opl, outer plexiform layer; onl. outer nuclear layer.

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

T Yvanka de Soysa¹^?, Allison Ulrich¹^?, Timo Friedrich², Danielle Pite¹, Shannon L Compton¹, Deborah Ok¹, Rebecca L Bernardos¹, Gerald B Downes², Shizuka Hsieh¹, Rachael Stein¹, M Caterina Lagdameo¹, Katherine Halvorsen¹, Lydia-Rose Kesich¹ and Michael JF Barresi¹^*

• * Corresponding author: Michael JF Barresi
• ? Equal contributors

Author Affiliations
<sup id="ins1">1</sup> Biological Sciences, Smith College, Northampton, MA 01063, USA
<sup id="ins2">2</sup> Molecular and Cellular Biology, University of Massachusetts, Amherst MA, USA

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BMC Biology 2012, 10:40 doi:10.1186/1741-7007-10-40

The electronic version of this article is the complete one and can be found online at: http://www.biomedcentral.com/1741-7007/10/40

<table cellpadding="0" cellspacing="0"> <tbody> <tr><td>Received:</td><td>30 March 2012</td></tr> <tr><td>Accepted:</td><td>4 May 2012</td></tr> <tr><td>Published:</td><td>4 May 2012</td></tr> </tbody> </table>
? 2012 de Soysa et al; licensee BioMed Central Ltd.

This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Abstract

Background

The 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.
Results

WAF 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.
Conclusions

Whether 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.
Keywords:

Deepwater Horizon; crude oil; zebrafish; embryonic development; cardiovascular; cartilage; neural crest; peripheral nervous system; somitogenesis; muscle

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