1. Neuroscience
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Magnetosensitive neurons mediate geomagnetic orientation in Caenorhabditis elegans

  1. Andrés Vidal-Gadea
  2. Kristi Ward
  3. Celia Beron
  4. Navid Ghorashian
  5. Sertan Gokce
  6. Joshua Russell
  7. Nicholas Truong
  8. Adhishri Parikh
  9. Otilia Gadea
  10. Adela Ben-Yakar
  11. Jonathan Pierce-Shimomura  Is a corresponding author
  1. Illinois State University, United States
  2. University of Texas at Austin, United States
Research Article
  • Cited 53
  • Views 12,202
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Cite this article as: eLife 2015;4:e07493 doi: 10.7554/eLife.07493

Abstract

Many organisms spanning from bacteria to mammals orient to the earth's magnetic field. For a few animals, central neurons responsive to earth-strength magnetic fields have been identified; however, magnetosensory neurons have yet to be identified in any animal. We show that the nematode Caenorhabditis elegans orients to the earth's magnetic field during vertical burrowing migrations. Well-fed worms migrated up, while starved worms migrated down. Populations isolated from around the world, migrated at angles to the magnetic vector that would optimize vertical translation in their native soil, with northern- and southern-hemisphere worms displaying opposite migratory preferences. Magnetic orientation and vertical migrations required the TAX-4 cyclic nucleotide-gated ion channel in the AFD sensory neuron pair. Calcium imaging showed that these neurons respond to magnetic fields even without synaptic input. C. elegans may have adapted magnetic orientation to simplify their vertical burrowing migration by reducing the orientation task from three dimensions to one.

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Author details

  1. Andrés Vidal-Gadea

    School of Biological Sciences, Illinois State University, Normal, United States
    Competing interests
    The authors declare that no competing interests exist.

  2. Kristi Ward

    Department of Neuroscience; Center for Brain, Behavior and Evolution; Center for Learning and Memory; Waggoner Center for Alcohol and Addiction Research; Institute of Cell and Molecular Biology, University of Texas at Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.

  3. Celia Beron

    Department of Neuroscience; Center for Brain, Behavior and Evolution; Center for Learning and Memory; Waggoner Center for Alcohol and Addiction Research; Institute of Cell and Molecular Biology, University of Texas at Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.

  4. Navid Ghorashian

    Department of Mechanical Engineering, University of Texas at Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.

  5. Sertan Gokce

    Department of Electrical Engineering, University of Texas at Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.

  6. Joshua Russell

    Department of Neuroscience; Center for Brain, Behavior and Evolution; Center for Learning and Memory; Waggoner Center for Alcohol and Addiction Research; Institute of Cell and Molecular Biology, University of Texas at Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.

  7. Nicholas Truong

    Department of Neuroscience; Center for Brain, Behavior and Evolution; Center for Learning and Memory; Waggoner Center for Alcohol and Addiction Research; Institute of Cell and Molecular Biology, University of Texas at Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.

  8. Adhishri Parikh

    Department of Neuroscience; Center for Brain, Behavior and Evolution; Center for Learning and Memory; Waggoner Center for Alcohol and Addiction Research; Institute of Cell and Molecular Biology, University of Texas at Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.

  9. Otilia Gadea

    Department of Neuroscience; Center for Brain, Behavior and Evolution; Center for Learning and Memory; Waggoner Center for Alcohol and Addiction Research; Institute of Cell and Molecular Biology, University of Texas at Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.

  10. Adela Ben-Yakar

    Department of Mechanical Engineering, University of Texas at Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.

  11. Jonathan Pierce-Shimomura

    Department of Neuroscience; Center for Brain, Behavior and Evolution; Center for Learning and Memory; Waggoner Center for Alcohol and Addiction Research; Institute of Cell and Molecular Biology, University of Texas at Austin, Austin, United States
    For correspondence
    jonps@austin.utexas.edu
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. Russ Fernald, Stanford University, United States

Publication history

  1. Received: March 15, 2015
  2. Accepted: June 16, 2015
  3. Accepted Manuscript published: June 17, 2015 (version 1)
  4. Version of Record published: August 5, 2015 (version 2)

Copyright

© 2015, Vidal-Gadea et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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Further reading

    1. Neuroscience

    Response to comment on "Magnetosensitive neurons mediate geomagnetic orientation in Caenorhabditis elegans"

    Andres Vidal-Gadea et al.
    Scientific Correspondence

    Many animals can orient using the earth’s magnetic field. In a recent study, we performed three distinct behavioral assays providing evidence that the nematode Caenorhabditis elegans orients to earth-strength magnetic fields (Vidal-Gadea et al., 2015). A new study by Landler et al. suggests that C. elegans does not orient to magnetic fields (Landler et al., 2018). They also raise conceptual issues that cast doubt on our study. Here, we explain how they appear to have missed positive results in part by omitting controls and running assays longer than prescribed, so that worms switched their preferred migratory direction within single tests. We also highlight differences in experimental methods and interpretations that may explain our different results and conclusions. Together, these findings provide guidance on how to achieve robust magnetotaxis and reinforce our original finding that C. elegans is a suitable model system to study magnetoreception.

    1. Neuroscience

    Comment on "Magnetosensitive neurons mediate geomagnetic orientation in Caenorhabditis elegans"

    Lukas Landler et al.
    Scientific Correspondence

    A diverse array of species on the planet employ the Earth's magnetic field as a navigational aid. As the majority of these animals are migratory, their utility to interrogate the molecular and cellular basis of the magnetic sense is limited. Vidal-Gadea and colleagues recently argued that the worm Caenorhabditis elegans possesses a magnetic sense that guides their vertical movement in soil. In making this claim, they relied on three different behavioral assays that involved magnetic stimuli. Here, we set out to replicate their results employing blinded protocols and double wrapped coils that control for heat generation. We find no evidence supporting the existence of a magnetic sense in C. elegans. We further show that the Vidal-Gadea hypothesis is problematic as the adoption of a correction angle and a fixed trajectory relative to the Earth's magnetic inclination does not necessarily result in vertical movement.

    1. Neuroscience

    Magnetosensation: Finding a worm's internal compass

    Catharine H Rankin, Conny H Lin
    Insight

    A pair of neurons is required for nematodes to be able to navigate using the Earth's magnetic field.

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