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

  1. Elin Sorhus  Is a corresponding author
  2. John Patrick Incardona
  3. Tomasz Furmanek
  4. Giles W Goetz
  5. Nathaniel L Scholz
  6. Sonnich Meier
  7. Rolf Brudvik Edvardsen
  8. Sissel Jentoft
  1. Institute of Marine Research, Norway
  2. Northwest Fisheries Science Center, United States
  3. University of Oslo, Norway

Abstract

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.

Data availability

The following data sets were generated
    1. Soerhus E
    2. Incardona J
    3. Scholz N
    4. Furmanek
    5. Meier S
    6. Edvardsen R
    7. Jentoft S
    (2016) Sequence data
    Publicly available at the NCBI Sequence Read Archive (accession no: PRJNA287744).

Article and author information

Author details

  1. Elin Sorhus

    Institute of Marine Research, Bergen, Norway
    For correspondence
    elin.sorhus@imr.no
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3542-4201
  2. John Patrick Incardona

    Environmental and Fisheries Science Division, Northwest Fisheries Science Center, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Tomasz Furmanek

    Institute of Marine Research, Bergen, Norway
    Competing interests
    The authors declare that no competing interests exist.
  4. Giles W Goetz

    Environmental and Fisheries Science Division, Northwest Fisheries Science Center, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Nathaniel L Scholz

    Environmental and Fisheries Science Division, Northwest Fisheries Science Center, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Sonnich Meier

    Institute of Marine Research, Bergen, Norway
    Competing interests
    The authors declare that no competing interests exist.
  7. Rolf Brudvik Edvardsen

    Institute of Marine Research, Bergen, Norway
    Competing interests
    The authors declare that no competing interests exist.
  8. Sissel Jentoft

    Centre for Ecological and Evolutionary Synthesis, University of Oslo, Oslo, Norway
    Competing interests
    The authors declare that no competing interests exist.

Funding

Research Council of Norway (Project no. 234367)

  • Elin Sorhus
  • John Patrick Incardona
  • Tomasz Furmanek
  • Nathaniel L Scholz
  • Sonnich Meier
  • Rolf Brudvik Edvardsen

VISTA foundation (Project no. 6161)

  • Elin Sorhus

Institute of Marine Research (Project no. 14236)

  • Elin Sorhus
  • Tomasz Furmanek
  • Sonnich Meier
  • Rolf Brudvik Edvardsen

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Marianne Bronner, California Institute of Technology, United States

Ethics

Animal experimentation: All animal experiments within the study were approved by NARA, the governmental Norwegian Animal Research Authority (http://www.fdu.no/fdu/, reference number 2012/275334-2). All methods were performed in accordance with approved guidelines.

Version history

  1. Received: August 26, 2016
  2. Accepted: January 20, 2017
  3. Accepted Manuscript published: January 24, 2017 (version 1)
  4. Version of Record published: February 10, 2017 (version 2)

Copyright

This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

Metrics

  • 1,804
    views
  • 299
    downloads
  • 85
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Elin Sorhus
  2. John Patrick Incardona
  3. Tomasz Furmanek
  4. Giles W Goetz
  5. Nathaniel L Scholz
  6. Sonnich Meier
  7. Rolf Brudvik Edvardsen
  8. Sissel Jentoft
(2017)
Novel adverse outcome pathways revealed by chemical genetics in a developing marine fish
eLife 6:e20707.
https://doi.org/10.7554/eLife.20707

Share this article

https://doi.org/10.7554/eLife.20707

Further reading

    1. Computational and Systems Biology
    2. Ecology
    Kazushi Tsutsui, Ryoya Tanaka ... Keisuke Fujii
    Research Article

    Collaborative hunting, in which predators play different and complementary roles to capture prey, has been traditionally believed to be an advanced hunting strategy requiring large brains that involve high-level cognition. However, recent findings that collaborative hunting has also been documented in smaller-brained vertebrates have placed this previous belief under strain. Here, using computational multi-agent simulations based on deep reinforcement learning, we demonstrate that decisions underlying collaborative hunts do not necessarily rely on sophisticated cognitive processes. We found that apparently elaborate coordination can be achieved through a relatively simple decision process of mapping between states and actions related to distance-dependent internal representations formed by prior experience. Furthermore, we confirmed that this decision rule of predators is robust against unknown prey controlled by humans. Our computational ecological results emphasize that collaborative hunting can emerge in various intra- and inter-specific interactions in nature, and provide insights into the evolution of sociality.

    1. Ecology
    2. Evolutionary Biology
    Théo Constant, F Stephen Dobson ... Sylvain Giroud
    Research Article

    Seasonal animal dormancy is widely interpreted as a physiological response for surviving energetic challenges during the harshest times of the year (the physiological constraint hypothesis). However, there are other mutually non-exclusive hypotheses to explain the timing of animal dormancy, that is, entry into and emergence from hibernation (i.e. dormancy phenology). Survival advantages of dormancy that have been proposed are reduced risks of predation and competition (the ‘life-history’ hypothesis), but comparative tests across animal species are few. Using the phylogenetic comparative method applied to more than 20 hibernating mammalian species, we found support for both hypotheses as explanations for the phenology of dormancy. In accordance with the life-history hypotheses, sex differences in hibernation emergence and immergence were favored by the sex difference in reproductive effort. In addition, physiological constraint may influence the trade-off between survival and reproduction such that low temperatures and precipitation, as well as smaller body mass, influence sex differences in phenology. We also compiled initial evidence that ectotherm dormancy may be (1) less temperature dependent than previously thought and (2) associated with trade-offs consistent with the life-history hypothesis. Thus, dormancy during non-life-threatening periods that are unfavorable for reproduction may be more widespread than previously thought.