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Magnetosensitive neurons mediate geomagnetic orientation in Caenorhabditis elegans.

Vidal-Gadea A, Ward K, Beron C, Ghorashian N, Gokce S, Russell J, Truong N, Parikh A, Gadea O, Ben-Yakar A, Pierce-Shimomura J - Elife (2015)

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: 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.

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.

No MeSH data available.


A new assay for testing magnetotactic ability.(A) We developed a convenient assay able to determine the ability of worm populations to detect and orient to magnetic fields. Worms were placed in the center of an agar plate. A 1.5 μl drop of anesthetic (NaN3) was placed at the center of two test areas equidistant from the start, and a magnet was then centered above one of the two test areas. We calculated the magnetotaxis index as: Magnetotaxis Index = (M − C)/(M + C). Where M is the number of worms found immobilized by the test area at the magnet, and C is the number of worms immobilized by the control test area. (B) If no magnet was present, worms distributed evenly between the two test areas. If a magnet was introduced above one of the areas, about two thirds of the worms preferentially migrated to the magnet test area. We repeated the experiment in assay plates wrapped in several layers of aluminum foil and observed that migration towards the magnet did not require light.DOI:http://dx.doi.org/10.7554/eLife.07493.009
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fig4s1: A new assay for testing magnetotactic ability.(A) We developed a convenient assay able to determine the ability of worm populations to detect and orient to magnetic fields. Worms were placed in the center of an agar plate. A 1.5 μl drop of anesthetic (NaN3) was placed at the center of two test areas equidistant from the start, and a magnet was then centered above one of the two test areas. We calculated the magnetotaxis index as: Magnetotaxis Index = (M − C)/(M + C). Where M is the number of worms found immobilized by the test area at the magnet, and C is the number of worms immobilized by the control test area. (B) If no magnet was present, worms distributed evenly between the two test areas. If a magnet was introduced above one of the areas, about two thirds of the worms preferentially migrated to the magnet test area. We repeated the experiment in assay plates wrapped in several layers of aluminum foil and observed that migration towards the magnet did not require light.DOI:http://dx.doi.org/10.7554/eLife.07493.009

Mentions: The results of our magnetic coil and burrowing experiments suggested that worms use the local magnetic field to guide vertical migrations. Unfortunately these experiments are limited to a few assays at the time, preventing their use in larger-scale behavioral screens. To mitigate this shortcoming, we developed a new assay using strong rare-earth magnets to quickly assess the ability of different strains to respond to imposed magnetic fields (Figure 4A). This assay allowed us to run many assays at the same time. Briefly, worms were placed at the center of an assay plate and allowed to migrate freely (Figure 4A, and ‘Materials and methods’). A magnet was then placed above one of two equidistant ‘goal’ areas. Magnetotactic performance was quantified with a magnetotaxis index computed as the difference between the number of worms reaching either goal divided by the number of worms reaching both goals. We found that when no magnet was present, worms distributed evenly between these two goals. However, if the magnet was present, worms preferentially migrated toward it (Figure 4—figure supplement 1, Supplementary file 1A). To ensure the presence of the magnet did not introduce an unwanted thermal gradient, we recorded the temperature difference between goals in the presence and absence of a magnet and found that the two treatments did not significantly differ from each other (Figure 2—figure supplement 1C,D). We used this assay to compare the ability of different strains to detect and migrate in a biased way in the presence of strong magnetic field. We first turned our attention to many wild C. elegans strains isolated from different locations across the world.10.7554/eLife.07493.008Figure 4.Magnetotactic variability between wild C. elegans isolates result from differences in local magnetic field properties.


Magnetosensitive neurons mediate geomagnetic orientation in Caenorhabditis elegans.

Vidal-Gadea A, Ward K, Beron C, Ghorashian N, Gokce S, Russell J, Truong N, Parikh A, Gadea O, Ben-Yakar A, Pierce-Shimomura J - Elife (2015)

A new assay for testing magnetotactic ability.(A) We developed a convenient assay able to determine the ability of worm populations to detect and orient to magnetic fields. Worms were placed in the center of an agar plate. A 1.5 μl drop of anesthetic (NaN3) was placed at the center of two test areas equidistant from the start, and a magnet was then centered above one of the two test areas. We calculated the magnetotaxis index as: Magnetotaxis Index = (M − C)/(M + C). Where M is the number of worms found immobilized by the test area at the magnet, and C is the number of worms immobilized by the control test area. (B) If no magnet was present, worms distributed evenly between the two test areas. If a magnet was introduced above one of the areas, about two thirds of the worms preferentially migrated to the magnet test area. We repeated the experiment in assay plates wrapped in several layers of aluminum foil and observed that migration towards the magnet did not require light.DOI:http://dx.doi.org/10.7554/eLife.07493.009
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4525075&req=5

fig4s1: A new assay for testing magnetotactic ability.(A) We developed a convenient assay able to determine the ability of worm populations to detect and orient to magnetic fields. Worms were placed in the center of an agar plate. A 1.5 μl drop of anesthetic (NaN3) was placed at the center of two test areas equidistant from the start, and a magnet was then centered above one of the two test areas. We calculated the magnetotaxis index as: Magnetotaxis Index = (M − C)/(M + C). Where M is the number of worms found immobilized by the test area at the magnet, and C is the number of worms immobilized by the control test area. (B) If no magnet was present, worms distributed evenly between the two test areas. If a magnet was introduced above one of the areas, about two thirds of the worms preferentially migrated to the magnet test area. We repeated the experiment in assay plates wrapped in several layers of aluminum foil and observed that migration towards the magnet did not require light.DOI:http://dx.doi.org/10.7554/eLife.07493.009
Mentions: The results of our magnetic coil and burrowing experiments suggested that worms use the local magnetic field to guide vertical migrations. Unfortunately these experiments are limited to a few assays at the time, preventing their use in larger-scale behavioral screens. To mitigate this shortcoming, we developed a new assay using strong rare-earth magnets to quickly assess the ability of different strains to respond to imposed magnetic fields (Figure 4A). This assay allowed us to run many assays at the same time. Briefly, worms were placed at the center of an assay plate and allowed to migrate freely (Figure 4A, and ‘Materials and methods’). A magnet was then placed above one of two equidistant ‘goal’ areas. Magnetotactic performance was quantified with a magnetotaxis index computed as the difference between the number of worms reaching either goal divided by the number of worms reaching both goals. We found that when no magnet was present, worms distributed evenly between these two goals. However, if the magnet was present, worms preferentially migrated toward it (Figure 4—figure supplement 1, Supplementary file 1A). To ensure the presence of the magnet did not introduce an unwanted thermal gradient, we recorded the temperature difference between goals in the presence and absence of a magnet and found that the two treatments did not significantly differ from each other (Figure 2—figure supplement 1C,D). We used this assay to compare the ability of different strains to detect and migrate in a biased way in the presence of strong magnetic field. We first turned our attention to many wild C. elegans strains isolated from different locations across the world.10.7554/eLife.07493.008Figure 4.Magnetotactic variability between wild C. elegans isolates result from differences in local magnetic field properties.

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: 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.

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.

No MeSH data available.