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Regulation of hyperoxia-induced social behaviour in Pristionchus pacificus nematodes requires a novel cilia-mediated environmental input

Social behaviours are frequently utilised for defence and stress avoidance in nature. Both Caenorhabditis elegans and Pristionchus pacificus nematodes display social behaviours including clumping and bordering, to avoid hyperoxic stress conditions. Additionally, both species show natural variation i...

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Autores principales: Moreno, Eduardo, Sieriebriennikov, Bogdan, Witte, Hanh, Rödelsperger, Christian, Lightfoot, James W., Sommer, Ralf J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5730589/
https://www.ncbi.nlm.nih.gov/pubmed/29242625
http://dx.doi.org/10.1038/s41598-017-18019-0
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author Moreno, Eduardo
Sieriebriennikov, Bogdan
Witte, Hanh
Rödelsperger, Christian
Lightfoot, James W.
Sommer, Ralf J.
author_facet Moreno, Eduardo
Sieriebriennikov, Bogdan
Witte, Hanh
Rödelsperger, Christian
Lightfoot, James W.
Sommer, Ralf J.
author_sort Moreno, Eduardo
collection PubMed
description Social behaviours are frequently utilised for defence and stress avoidance in nature. Both Caenorhabditis elegans and Pristionchus pacificus nematodes display social behaviours including clumping and bordering, to avoid hyperoxic stress conditions. Additionally, both species show natural variation in social behaviours with “social” and “solitary” strains. While the single solitary C. elegans N2 strain has evolved under laboratory domestication due to a gain-of-function mutation in the neuropeptide receptor gene npr-1, P. pacificus solitary strains are commonplace and likely ancestral. P. pacificus therefore provides an opportunity to further our understanding of the mechanisms regulating these complex behaviours and how they evolved within an ecologically relevant system. Using CRISPR/Cas9 engineering, we show that Ppa-npr-1 has minimal influence on social behaviours, indicating independent evolutionary pathways compared to C. elegans. Furthermore, solitary P. pacificus strains show an unexpected locomotive response to hyperoxic conditions, suggesting a novel regulatory mechanism counteracting social behaviours. By utilising both forward and reverse genetic approaches we identified 10 genes of the intraflagellar transport machinery in ciliated neurons that are essential for this inhibition. Therefore, a novel cilia-mediated environmental input adds an additional level of complexity to the regulation of hyperoxia-induced social behaviours in P. pacificus, a mechanism unknown in C. elegans.
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spelling pubmed-57305892017-12-18 Regulation of hyperoxia-induced social behaviour in Pristionchus pacificus nematodes requires a novel cilia-mediated environmental input Moreno, Eduardo Sieriebriennikov, Bogdan Witte, Hanh Rödelsperger, Christian Lightfoot, James W. Sommer, Ralf J. Sci Rep Article Social behaviours are frequently utilised for defence and stress avoidance in nature. Both Caenorhabditis elegans and Pristionchus pacificus nematodes display social behaviours including clumping and bordering, to avoid hyperoxic stress conditions. Additionally, both species show natural variation in social behaviours with “social” and “solitary” strains. While the single solitary C. elegans N2 strain has evolved under laboratory domestication due to a gain-of-function mutation in the neuropeptide receptor gene npr-1, P. pacificus solitary strains are commonplace and likely ancestral. P. pacificus therefore provides an opportunity to further our understanding of the mechanisms regulating these complex behaviours and how they evolved within an ecologically relevant system. Using CRISPR/Cas9 engineering, we show that Ppa-npr-1 has minimal influence on social behaviours, indicating independent evolutionary pathways compared to C. elegans. Furthermore, solitary P. pacificus strains show an unexpected locomotive response to hyperoxic conditions, suggesting a novel regulatory mechanism counteracting social behaviours. By utilising both forward and reverse genetic approaches we identified 10 genes of the intraflagellar transport machinery in ciliated neurons that are essential for this inhibition. Therefore, a novel cilia-mediated environmental input adds an additional level of complexity to the regulation of hyperoxia-induced social behaviours in P. pacificus, a mechanism unknown in C. elegans. Nature Publishing Group UK 2017-12-14 /pmc/articles/PMC5730589/ /pubmed/29242625 http://dx.doi.org/10.1038/s41598-017-18019-0 Text en © The Author(s) 2017 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Moreno, Eduardo
Sieriebriennikov, Bogdan
Witte, Hanh
Rödelsperger, Christian
Lightfoot, James W.
Sommer, Ralf J.
Regulation of hyperoxia-induced social behaviour in Pristionchus pacificus nematodes requires a novel cilia-mediated environmental input
title Regulation of hyperoxia-induced social behaviour in Pristionchus pacificus nematodes requires a novel cilia-mediated environmental input
title_full Regulation of hyperoxia-induced social behaviour in Pristionchus pacificus nematodes requires a novel cilia-mediated environmental input
title_fullStr Regulation of hyperoxia-induced social behaviour in Pristionchus pacificus nematodes requires a novel cilia-mediated environmental input
title_full_unstemmed Regulation of hyperoxia-induced social behaviour in Pristionchus pacificus nematodes requires a novel cilia-mediated environmental input
title_short Regulation of hyperoxia-induced social behaviour in Pristionchus pacificus nematodes requires a novel cilia-mediated environmental input
title_sort regulation of hyperoxia-induced social behaviour in pristionchus pacificus nematodes requires a novel cilia-mediated environmental input
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5730589/
https://www.ncbi.nlm.nih.gov/pubmed/29242625
http://dx.doi.org/10.1038/s41598-017-18019-0
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