Magnetosensitive neurons mediate geomagnetic orientation in Caenorhabditis elegans.

Magnetosensitive neurons mediate geomagnetic orientation in Caenorhabditis elegans.
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DOI:
10.7554/elife.07493
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发表时间:
2015-06-17
期刊:
影响因子:
7.7
通讯作者:
Pierce-Shimomura J
Pierce-Shimomura J
中科院分区:
生物学1区
文献类型:
--
作者:
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

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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. DOI: http://dx.doi.org/10.7554/eLife.07493.001 The Earth has a magnetic field that protects the planet from the harmful effects of cosmic rays, which is generated by the movement of the layer of molten metal that surrounds the planet's solid inner core. The orientation of the magnetic field relative to the Earth's surface varies around the globe, and is like the pattern adopted by iron filings around a bar magnet. Many organisms, from bacteria to birds such as the Arctic Tern and mammals such as wolves, are able to exploit this variation in the Earth's magnetic field to help them navigate. In bacteria, this ability has been linked to the possession of tiny magnetic particles that align with the Earth's magnetic field lines. However, it is not clear how animals are able use the magnetic field to navigate. Vidal-Gadea et al. have now obtained clues to this process from a surprising source, namely a soil-dwelling nematode worm called Caenorhabiditis elegans. Worms that were placed inside a gelatin-filled cylinder preferred to burrow downward, but exposure to an artificial magnetic field that in effect reversed the Earth's magnetic field caused them to burrow upward. By contrast, worms that had been well-fed burrowed in the opposite direction. When worms were instead allowed to crawl across a flat surface with a parallel magnetic field, a map of the Earth's magnetic field revealed that the worms, which were originally from England but which were tested in the US, moved at an angle that would correspond—in England—to burrowing downwards when they were hungry and upwards when were not. Consistent with this, worms from Australia crawled in the opposite direction to English worms, setting off at an angle that would also be equivalent—in Australia—to downwards when hungry and upwards when full. Identical results were found for Hawaiian worms. Worms from countries on the Equator were less sensitive to magnetic fields than their northern and southern counterparts; which suggests that the response is genetically encoded. And indeed, a survey of mutant worms with defects in different neurons uncovered a pair of sensory neurons called ‘AFD neurons’ that serve the purpose of a compass, and allow the animals to navigate using geomagnetism. It remains unclear exactly how AFD neurons detect the Earth's magnetic field, and it is also not clear why hungry worms should burrow downwards while satisfied worms burrow upwards. One possibility is that hungry worms move downwards to feed on abundant but nutrient-poor bacteria growing on plant roots, whereas sated worms can afford to risk moving to the surface in search of more desirable, but less reliable, food sources. Future work could set out to test these explanations. DOI: http://dx.doi.org/10.7554/eLife.07493.002