Untangling mechanisms of crude oil toxicity: linking gene expression, morphology and PAHs at two developmental stages in a cold-water fish

Abstract

Early life stages of fish are highly sensitive to crude oil exposure and thus, short term exposures during critical developmental periods could have detrimental consequences for juvenile survival. Here we administered crude oil to Atlantic haddock (Melanogrammus aeglefinus) in short term (3-day) exposures at two developmental time periods: before first heartbeat, from gastrulation to cardiac cone stage (early), and from first heartbeat to one day before hatching (late). A frequent sampling regime enabled us to determine immediate PAH uptake, metabolite formation and gene expression changes. In general, the embryotoxic consequences of an oil exposure were more severe in the early exposure animals. Oil droplet fouling in the highest doses resulted in severe cardiac and craniofacial abnormalities. Gene expression changes of Cytochrome 1 a,b,c and d (cyp1a,b,c,d), Bone morphogenetic protein 10 (bmp10), ABC transporter b1 (abcb1) and Rh-associated G-protein (rhag) were linked to PAH uptake, occurrence of metabolites of phenanthrene and developmental and functional abnormalities. We detected circulation-independent, oil-induced gene expression changes and separated phenotypes linked to proliferation, growth and disruption of formation events at early and late developmental stages. Our study gives an increased knowledge about developmentally dependent effects of crude oil toxicity. Thus, providing more knowledge and detail to new and several existing adverse outcome pathways of crude oil toxicity. Graphical abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=93 SRC="FIGDIR/small/288852v2_ufig1.gif" ALT="Figure 1"> View larger version (35K): org.highwire.dtl.DTLVardef@106fe07org.highwire.dtl.DTLVardef@f8d7borg.highwire.dtl.DTLVardef@1118852org.highwire.dtl.DTLVardef@ccc59_HPS_FORMAT_FIGEXP M_FIG C_FIG HighlightsO_LIOil droplet fouling occurred in the whole water column and increased the oil toxicity. C_LIO_LIEarly exposure resulted in higher PAH uptake due to lower metabolism resulting in more severe abnormalities. C_LIO_LIA rapid and circulation-indepenent regulation of bmp10 suggested a direct oil-induced effect on calcium homeostasis. C_LIO_LIExpression of rhag indicated a direct oil-induced effect on osmoregulatory cells and osmoregulation. C_LIO_LISevere eye abnormalities especially in the late exposure was linked to inappropriate overexpression of cyp1b in the eyes. C_LI