Multiple Chemosensory Neurons Mediate Avoidance Behavior to Rare Earth Ions in Caenorhabditis elegans
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Multiple Chemosensory Neurons Mediate Avoidance Behavior to Rare Earth Ions in Caenorhabditis elegans Tokumitsu Wakabayashi 1
&
Yui Nojiri 1 & Miwa Takahashi-Watanabe 1
Received: 16 June 2020 / Accepted: 2 September 2020 # Springer Science+Business Media, LLC, part of Springer Nature 2020
Abstract As rare earth (RE) metals are abundantly present in the soil, in spite of their name, it is conceivable that organisms may encounter and interact with RE ions. In the present study, we demonstrated that the soil nematode Caenorhabditis elegans avoids RE ions, such as yttrium and all examined lanthanide ions, which exhibit toxic effects on nematodes. We also demonstrated that the chemosensory system of this animal mediates avoidance behavior toward RE ions similar to heavy metal (HM) ion avoidance. The C. elegans dyf-11(pe554) mutant is unable to respond to chemosensory cues because it lacks all ciliated endings of the chemosensory neurons required for the detection of environmental chemicals. Cell-specific rescue of the dyf-11 mutant and cellspecific genetic ablation studies revealed that the avoidance behavior toward HM and RE ions was mediated by a partially overlapping but distinct subset of chemosensory neurons (ASH, ADL, ASE, ADF, and ASK). With the help of multiple chemosensory neurons, worms may improve the fidelity of avoidance behavior to evade RE ions. Among the chemosensory neurons in C. elegans, ADF and ASK neurons were involved in RE avoidance, but not in HM avoidance. These results suggested that ADF and ASK neurons in C. elegans have RE-selective mechanisms to mediate the avoidance response. Keywords C. elegans . Rare earth ions . Toxicity . Avoidance behavior . Chemosensory function
Introduction Heavy metal (HM) ions are essential for cellular metabolism, as they function as co-factors in a variety of proteins, including respiratory enzymes. Organisms use metal ions that are abundantly present in the soil, such as Fe2+, Cu2+, and Zn2+. However, excess amounts of HMs are toxic to many organisms [1, 2]. Despite the name, rare earth (RE) elements, including scandium, yttrium, and lanthanides, are relatively abundant in soil. As these elements are readily available in the environment, it is conceivable that organisms encounter and interact with RE elements during their life cycle. Indeed, some RE ions are reported to be toxic to many organisms [3–7].
Electronic supplementary material The online version of this article (https://doi.org/10.1007/s12011-020-02375-6) contains supplementary material, which is available to authorized users. * Tokumitsu Wakabayashi [email protected] 1
Department of Chemistry and Biosciences, Faculty of Science and Engineering, Iwate University, 4-3-5 Ueda, Morioka 020-8551, Japan
Because of its ease of use, short life cycle, simple nervous system, and many genetic tools available, the soil nematode, Caenorhabditis elegans, has been widely used as an animal model in many aspects of biological studies including metal toxicity [8–12] and chemosensory behavior [8, 13–15]. Previo
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