Journal Article

Novel adverse outcome pathways revealed by chemical genetics in a developing marine fish

Scholz, Nathaniel L, Goetz, Giles W, Furmanek, Tomasz, Meier, Sonnich, Sørhus, Elin, Incardona, John P, Edvardsen, Rolf B, Jentoft, Sissel

2017

Overview

Crude oil spills are a worldwide ocean conservation threat. Fish are particularly vulnerable to the oiling of spawning habitats, and crude oil causes severe abnormalities in embryos and larvae. However, the underlying mechanisms for these developmental defects are not well understood. Here, we explore the transcriptional basis for four discrete crude oil injury phenotypes in the early life stages of the commercially important Atlantic haddock (Melanogrammus aeglefinus). These include defects in (1) cardiac form and function, (2) craniofacial development, (3) ionoregulation and fluid balance, and (4) cholesterol synthesis and homeostasis. Our findings suggest a key role for intracellular calcium cycling and excitation-transcription coupling in the dysregulation of heart and jaw morphogenesis. Moreover, the disruption of ionoregulatory pathways sheds new light on buoyancy control in marine fish embryos. Overall, our chemical-genetic approach identifies initiating events for distinct adverse outcome pathways and novel roles for individual genes in fundamental developmental processes. Accidental oil spills are a worldwide threat to ocean life. Fish eggs and larvae are especially vulnerable; therefore oil spills in areas where fish spawn are of great concern. Fish embryos exposed to crude oil grow slower than normal as larvae and juveniles and often show defects in the heart, face and jaw. However, the underlying mechanisms behind these defects are largely unknown. Working with the Atlantic haddock (Melanogrammus aeglefinus), Sørhus et al. have now examined fish embryos and larvae that had been exposed to crude oil, and identified those genes that were more active or less active than normal. The findings add further support to the idea that exposure to crude oil causes heart and face defects because it interferes with how the cells that develop into these structures use calcium ions. Signals sent via calcium ions are not only important for the contraction of muscle cells, but they are also essential for regulation of some genes. So, by interfering with the circulation of calcium ions, crude oil can have consequences for both how muscles work and how genes are regulated. Sørhus et al. also report two previously uncharacterized defects. Firstly, genes that help to regulate the ion and water content of the tissues were highly affected in young fish exposed to crude oil. Some of the genes were more active than normal, while others were less active. This finding in particular would explain why oil-exposed embryos often accumulate fluids, and suggests that the larvae may have altered buoyancy too. Secondly, the oil-exposed embryos showed signs of a shortage of cholesterol and other fatty molecules. This is most likely because they absorbed less material from their yolk, which could also explain why larvae exposed to crude oil grow more slowly than normal. Finally, in the future, these newly identified genes connected to crude oil toxicity could be used as diagnostic markers to confirm oil-induced injury in fish, and monitor the health of fish populations in the ocean.

• Publisher: eLife Sciences Publications Ltd,eLife Sciences Publications, Ltd
• Subject: Animals / Aquatic Organisms - drug effects / Atlantic haddock / Calcium (intracellular) / cardiac abnormalities / chemical genetics / Chemical spills / Cholesterol / craniofacial abnormalities / Craniofacial growth / Crude oil / Datasets / Defects / Ecology / Edema / Embryos / Fish / Fish oils / Fisheries / Gadiformes - embryology / Gadinae / Gene expression / Genomics and Evolutionary Biology / Heart / Heart diseases / Homeostasis / Jaw / Morphogenesis / Morphogenesis - drug effects / Morphology / Oil spills / Petroleum - toxicity / Petroleum production / Physiology / Risk assessment / Spawning / Transcription / transcriptome / Water Pollutants - toxicity / Zebrafish