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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.


Genetic ablation of AFD does not impair chemotaxis.(A) Genetic ablation of the AFD neurons did not impair the ability of worms to move, or orient to the chemical attractant diacetyl compared to control sister worms that did not carry a cell-death transgene (ICE). Comparison between the AFD neurons of animals expressing GFP (B), or GFP and ICE (C), revealed that in animals expressing the cell-death gene the AFD neuron is impaired and shows many of the typical signs of neurodegeneration (e.g., circular soma, beaded and fragmented processes).DOI:http://dx.doi.org/10.7554/eLife.07493.012
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fig6s1: Genetic ablation of AFD does not impair chemotaxis.(A) Genetic ablation of the AFD neurons did not impair the ability of worms to move, or orient to the chemical attractant diacetyl compared to control sister worms that did not carry a cell-death transgene (ICE). Comparison between the AFD neurons of animals expressing GFP (B), or GFP and ICE (C), revealed that in animals expressing the cell-death gene the AFD neuron is impaired and shows many of the typical signs of neurodegeneration (e.g., circular soma, beaded and fragmented processes).DOI:http://dx.doi.org/10.7554/eLife.07493.012

Mentions: To test the requirement of the AFD neuron pair in magnetosensation, we genetically ablated them via cell-specific expression of a transgene for a human cell-death caspase. One advantage of this technique is that only a fraction of individual worms will inherit the artificial chromosome carrying the transgene. This allowed us to compare the performance of sister worms grown and tested together under identical conditions and only differing in having or not said transgene. After each assay, individual worms with genetically ablated neurons were distinguished from their unaffected sisters by the co-expression of a fluorescent transgene reporter. We found that worms lacking the AFD sensory neurons failed to orient to an artificial magnetic field, while their unaffected sisters oriented normally (Figure 6A, Supplementary file 1A). This could not be explained by non-specific defects, because these worms could move and orient normally to olfactory stimuli (Figure 6—figure supplement 1). Similarly ablating nearby sensory neuron pairs ASE and AWC had no effect on magnetotaxis. The sensory ending of the AFD neurons consists of dozens of villi arranged anterior-to-posterior (in an antenna-like formation) imbedded inside glial cells (Perkins et al., 1986; Doroquez et al., 2014). Genetic ablation of the glia surrounding these structures, results in worms with viable AFD neurons but lacking villi (Bacaj et al., 2008). These worms were unable to orient to artificial magnetic fields (Figure 6A). This supports the idea that the villi may be the site of magneto-transduction (and/or that the glia themselves contribute to this sense). Taken together, our results demonstrate that the AFD sensory neurons are required for magnetotaxis.10.7554/eLife.07493.011Figure 6.Geomagnetotaxis requires the TAX-4/TAX-2 cGMP-gated ion channel in the AFD sensory neurons.


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)

Genetic ablation of AFD does not impair chemotaxis.(A) Genetic ablation of the AFD neurons did not impair the ability of worms to move, or orient to the chemical attractant diacetyl compared to control sister worms that did not carry a cell-death transgene (ICE). Comparison between the AFD neurons of animals expressing GFP (B), or GFP and ICE (C), revealed that in animals expressing the cell-death gene the AFD neuron is impaired and shows many of the typical signs of neurodegeneration (e.g., circular soma, beaded and fragmented processes).DOI:http://dx.doi.org/10.7554/eLife.07493.012
© Copyright Policy
Related In: Results  -  Collection

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

fig6s1: Genetic ablation of AFD does not impair chemotaxis.(A) Genetic ablation of the AFD neurons did not impair the ability of worms to move, or orient to the chemical attractant diacetyl compared to control sister worms that did not carry a cell-death transgene (ICE). Comparison between the AFD neurons of animals expressing GFP (B), or GFP and ICE (C), revealed that in animals expressing the cell-death gene the AFD neuron is impaired and shows many of the typical signs of neurodegeneration (e.g., circular soma, beaded and fragmented processes).DOI:http://dx.doi.org/10.7554/eLife.07493.012
Mentions: To test the requirement of the AFD neuron pair in magnetosensation, we genetically ablated them via cell-specific expression of a transgene for a human cell-death caspase. One advantage of this technique is that only a fraction of individual worms will inherit the artificial chromosome carrying the transgene. This allowed us to compare the performance of sister worms grown and tested together under identical conditions and only differing in having or not said transgene. After each assay, individual worms with genetically ablated neurons were distinguished from their unaffected sisters by the co-expression of a fluorescent transgene reporter. We found that worms lacking the AFD sensory neurons failed to orient to an artificial magnetic field, while their unaffected sisters oriented normally (Figure 6A, Supplementary file 1A). This could not be explained by non-specific defects, because these worms could move and orient normally to olfactory stimuli (Figure 6—figure supplement 1). Similarly ablating nearby sensory neuron pairs ASE and AWC had no effect on magnetotaxis. The sensory ending of the AFD neurons consists of dozens of villi arranged anterior-to-posterior (in an antenna-like formation) imbedded inside glial cells (Perkins et al., 1986; Doroquez et al., 2014). Genetic ablation of the glia surrounding these structures, results in worms with viable AFD neurons but lacking villi (Bacaj et al., 2008). These worms were unable to orient to artificial magnetic fields (Figure 6A). This supports the idea that the villi may be the site of magneto-transduction (and/or that the glia themselves contribute to this sense). Taken together, our results demonstrate that the AFD sensory neurons are required for magnetotaxis.10.7554/eLife.07493.011Figure 6.Geomagnetotaxis requires the TAX-4/TAX-2 cGMP-gated ion channel in the AFD sensory neurons.

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.