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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.


Magnetotaxis requires intact AFD sensory neurons.We used our magnet assay to test a large number of sensory mutants. Mutations that impair the mechano- (mec-10), light- (lite-1), oxygen- (gcy-33), and taste- (che-1) sensory pathways spared magnetotaxis, while mutations in genes specifically required for AFD sensory neurons (ttx-1 and gcy-23,-8,-18) abolished magnetotaxis. Mutations that impair the cGMP-gated ion channel TAX-4/TAX-2 that are expressed in the AFD sensory neurons (and other cells) similarly prevented magnetotaxis.DOI:http://dx.doi.org/10.7554/eLife.07493.010
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fig5: Magnetotaxis requires intact AFD sensory neurons.We used our magnet assay to test a large number of sensory mutants. Mutations that impair the mechano- (mec-10), light- (lite-1), oxygen- (gcy-33), and taste- (che-1) sensory pathways spared magnetotaxis, while mutations in genes specifically required for AFD sensory neurons (ttx-1 and gcy-23,-8,-18) abolished magnetotaxis. Mutations that impair the cGMP-gated ion channel TAX-4/TAX-2 that are expressed in the AFD sensory neurons (and other cells) similarly prevented magnetotaxis.DOI:http://dx.doi.org/10.7554/eLife.07493.010

Mentions: To investigate the neuromolecular substrates for magnetosensation, we tested mutants with deficiencies in a variety of previously characterized sensory pathways. Mutants with severe defects in some sensory modalities displayed normal or nearly normal magnetic orientation (Figure 5). These included worms deficient in the touch-form of mechanosensation (mec-10, Arnadottir et al., 2011), light detection (lite-1, Edwards et al., 2008), taste (che-1, Uchida et al., 2003), and oxygen sensation (gcy-33, Zimmer et al., 2009). However, we also found mutants that were significantly impaired in magnetotaxis. This group comprised worms with mutations in genes co-expressed in a single sensory neuron pair called AFD, first implicated in thermosensation (Mori, 1999). These included two independent mutant alleles of ttx-1, important for AFD differentiation, and the triple mutant lacking guanylyl cyclases, gcy-23, gcy-8, and gcy-18, which together are critical for AFD function. Furthermore, we identified a set of transduction mutants that failed to perform magnetic orientation. These included two independent mutant alleles of each tax-4 and tax-2 genes. These encode subunits of a cGMP-gated ion channel already implicated in sensory transduction in many sensory neurons, including AFD (Komatsu et al., 1996).10.7554/eLife.07493.010Figure 5.Magnetotaxis requires intact 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)

Magnetotaxis requires intact AFD sensory neurons.We used our magnet assay to test a large number of sensory mutants. Mutations that impair the mechano- (mec-10), light- (lite-1), oxygen- (gcy-33), and taste- (che-1) sensory pathways spared magnetotaxis, while mutations in genes specifically required for AFD sensory neurons (ttx-1 and gcy-23,-8,-18) abolished magnetotaxis. Mutations that impair the cGMP-gated ion channel TAX-4/TAX-2 that are expressed in the AFD sensory neurons (and other cells) similarly prevented magnetotaxis.DOI:http://dx.doi.org/10.7554/eLife.07493.010
© Copyright Policy
Related In: Results  -  Collection

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

fig5: Magnetotaxis requires intact AFD sensory neurons.We used our magnet assay to test a large number of sensory mutants. Mutations that impair the mechano- (mec-10), light- (lite-1), oxygen- (gcy-33), and taste- (che-1) sensory pathways spared magnetotaxis, while mutations in genes specifically required for AFD sensory neurons (ttx-1 and gcy-23,-8,-18) abolished magnetotaxis. Mutations that impair the cGMP-gated ion channel TAX-4/TAX-2 that are expressed in the AFD sensory neurons (and other cells) similarly prevented magnetotaxis.DOI:http://dx.doi.org/10.7554/eLife.07493.010
Mentions: To investigate the neuromolecular substrates for magnetosensation, we tested mutants with deficiencies in a variety of previously characterized sensory pathways. Mutants with severe defects in some sensory modalities displayed normal or nearly normal magnetic orientation (Figure 5). These included worms deficient in the touch-form of mechanosensation (mec-10, Arnadottir et al., 2011), light detection (lite-1, Edwards et al., 2008), taste (che-1, Uchida et al., 2003), and oxygen sensation (gcy-33, Zimmer et al., 2009). However, we also found mutants that were significantly impaired in magnetotaxis. This group comprised worms with mutations in genes co-expressed in a single sensory neuron pair called AFD, first implicated in thermosensation (Mori, 1999). These included two independent mutant alleles of ttx-1, important for AFD differentiation, and the triple mutant lacking guanylyl cyclases, gcy-23, gcy-8, and gcy-18, which together are critical for AFD function. Furthermore, we identified a set of transduction mutants that failed to perform magnetic orientation. These included two independent mutant alleles of each tax-4 and tax-2 genes. These encode subunits of a cGMP-gated ion channel already implicated in sensory transduction in many sensory neurons, including AFD (Komatsu et al., 1996).10.7554/eLife.07493.010Figure 5.Magnetotaxis requires intact 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.