Roles of the ClC chloride channel CLH-1 in food-associated salt chemotaxis behavior of C. elegans

The ability of animals to process dynamic sensory information facilitates foraging in an ever-changing environment. However, molecular and neural mechanisms underlying such ability remain elusive. The ClC anion channels/transporters play a pivotal role in cellular ion homeostasis across all phyla. H...

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Main Authors: Chanhyun Park, Yuki Sakurai, Hirofumi Sato, Shinji Kanda, Yuichi Iino, Hirofumi Kunitomo
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2021-01-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/55701
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author Chanhyun Park
Yuki Sakurai
Hirofumi Sato
Shinji Kanda
Yuichi Iino
Hirofumi Kunitomo
author_facet Chanhyun Park
Yuki Sakurai
Hirofumi Sato
Shinji Kanda
Yuichi Iino
Hirofumi Kunitomo
author_sort Chanhyun Park
collection DOAJ
description The ability of animals to process dynamic sensory information facilitates foraging in an ever-changing environment. However, molecular and neural mechanisms underlying such ability remain elusive. The ClC anion channels/transporters play a pivotal role in cellular ion homeostasis across all phyla. Here, we find a ClC chloride channel is involved in salt concentration chemotaxis of Caenorhabditis elegans. Genetic screening identified two altered-function mutations of clh-1 that disrupt experience-dependent salt chemotaxis. Using genetically encoded fluorescent sensors, we demonstrate that CLH-1 contributes to regulation of intracellular anion and calcium dynamics of salt-sensing neuron, ASER. The mutant CLH-1 reduced responsiveness of ASER to salt stimuli in terms of both temporal resolution and intensity, which disrupted navigation strategies for approaching preferred salt concentrations. Furthermore, other ClC genes appeared to act redundantly in salt chemotaxis. These findings provide insights into the regulatory mechanism of neuronal responsivity by ClCs that contribute to modulation of navigation behavior.
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spelling doaj.art-9e3f2afe30244652ae981b59313d996f2022-12-22T03:33:46ZengeLife Sciences Publications LtdeLife2050-084X2021-01-011010.7554/eLife.55701Roles of the ClC chloride channel CLH-1 in food-associated salt chemotaxis behavior of C. elegansChanhyun Park0https://orcid.org/0000-0002-0200-6903Yuki Sakurai1Hirofumi Sato2Shinji Kanda3Yuichi Iino4https://orcid.org/0000-0002-0936-2660Hirofumi Kunitomo5https://orcid.org/0000-0001-7312-7051Department of Biological Sciences, School of Science, The University of Tokyo, Tokyo, JapanDepartment of Biological Sciences, School of Science, The University of Tokyo, Tokyo, JapanDepartment of Biological Sciences, School of Science, The University of Tokyo, Tokyo, JapanDepartment of Biological Sciences, School of Science, The University of Tokyo, Tokyo, Japan; Laboratory of Physiology, Atmosphere and Ocean Research Institute, The University of Tokyo, Chiba, JapanDepartment of Biological Sciences, School of Science, The University of Tokyo, Tokyo, JapanDepartment of Biological Sciences, School of Science, The University of Tokyo, Tokyo, JapanThe ability of animals to process dynamic sensory information facilitates foraging in an ever-changing environment. However, molecular and neural mechanisms underlying such ability remain elusive. The ClC anion channels/transporters play a pivotal role in cellular ion homeostasis across all phyla. Here, we find a ClC chloride channel is involved in salt concentration chemotaxis of Caenorhabditis elegans. Genetic screening identified two altered-function mutations of clh-1 that disrupt experience-dependent salt chemotaxis. Using genetically encoded fluorescent sensors, we demonstrate that CLH-1 contributes to regulation of intracellular anion and calcium dynamics of salt-sensing neuron, ASER. The mutant CLH-1 reduced responsiveness of ASER to salt stimuli in terms of both temporal resolution and intensity, which disrupted navigation strategies for approaching preferred salt concentrations. Furthermore, other ClC genes appeared to act redundantly in salt chemotaxis. These findings provide insights into the regulatory mechanism of neuronal responsivity by ClCs that contribute to modulation of navigation behavior.https://elifesciences.org/articles/55701chloride channelchemotaxisadaptive behaviorsensory processing
spellingShingle Chanhyun Park
Yuki Sakurai
Hirofumi Sato
Shinji Kanda
Yuichi Iino
Hirofumi Kunitomo
Roles of the ClC chloride channel CLH-1 in food-associated salt chemotaxis behavior of C. elegans
eLife
chloride channel
chemotaxis
adaptive behavior
sensory processing
title Roles of the ClC chloride channel CLH-1 in food-associated salt chemotaxis behavior of C. elegans
title_full Roles of the ClC chloride channel CLH-1 in food-associated salt chemotaxis behavior of C. elegans
title_fullStr Roles of the ClC chloride channel CLH-1 in food-associated salt chemotaxis behavior of C. elegans
title_full_unstemmed Roles of the ClC chloride channel CLH-1 in food-associated salt chemotaxis behavior of C. elegans
title_short Roles of the ClC chloride channel CLH-1 in food-associated salt chemotaxis behavior of C. elegans
title_sort roles of the clc chloride channel clh 1 in food associated salt chemotaxis behavior of c elegans
topic chloride channel
chemotaxis
adaptive behavior
sensory processing
url https://elifesciences.org/articles/55701
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