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Consumption of Oleic Acid During Matriphagy in Free-Living Nematodes Alleviates the Toxic Effects of the Bacterial Metabolite Violacein

Maternal behaviors benefit the survival of young, contributing directly to the mother’s reproductive fitness. An extreme form of this is seen in matriphagy, when a mother performs the ultimate sacrifice and offers her body as a meal for her young. Whether matriphagy offers only a single energy-rich...

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Autores principales: Yoon, Kyoung-hye, Lee, Tong Young, Moon, Je-Hyun, Choi, Seong Yeol, Choi, Yun Ji, Mitchell, Robert J., Il Lee, Jin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7229185/
https://www.ncbi.nlm.nih.gov/pubmed/32415196
http://dx.doi.org/10.1038/s41598-020-64953-x
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author Yoon, Kyoung-hye
Lee, Tong Young
Moon, Je-Hyun
Choi, Seong Yeol
Choi, Yun Ji
Mitchell, Robert J.
Il Lee, Jin
author_facet Yoon, Kyoung-hye
Lee, Tong Young
Moon, Je-Hyun
Choi, Seong Yeol
Choi, Yun Ji
Mitchell, Robert J.
Il Lee, Jin
author_sort Yoon, Kyoung-hye
collection PubMed
description Maternal behaviors benefit the survival of young, contributing directly to the mother’s reproductive fitness. An extreme form of this is seen in matriphagy, when a mother performs the ultimate sacrifice and offers her body as a meal for her young. Whether matriphagy offers only a single energy-rich meal or another possible benefit to the young is unknown. Here, we characterized the toxicity of a bacterial secondary metabolite, namely, violacein, in Caenorhabditis elegans and found it is not only toxic towards adults, but also arrests growth and development of C. elegans larvae. To counteract this, C. elegans resorted to matriphagy, with the mothers holding their eggs within their bodies and hatching the young larvae internally, which eventually led to the mothers’ death. This violacein-induced matriphagy alleviated some of the toxic effects of violacein, allowing a portion of the internally-hatched young to bypass developmental arrest. Using genetic and pharmacological experiments, we found the consumption of oleate, a monounsaturated fatty acid produced by the mother, during matriphagy is partially responsible. As such, our study provides experimental evidence of why such a drastic and peculiar maternal behavior may have arisen in nematode natural habitats.
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spelling pubmed-72291852020-05-26 Consumption of Oleic Acid During Matriphagy in Free-Living Nematodes Alleviates the Toxic Effects of the Bacterial Metabolite Violacein Yoon, Kyoung-hye Lee, Tong Young Moon, Je-Hyun Choi, Seong Yeol Choi, Yun Ji Mitchell, Robert J. Il Lee, Jin Sci Rep Article Maternal behaviors benefit the survival of young, contributing directly to the mother’s reproductive fitness. An extreme form of this is seen in matriphagy, when a mother performs the ultimate sacrifice and offers her body as a meal for her young. Whether matriphagy offers only a single energy-rich meal or another possible benefit to the young is unknown. Here, we characterized the toxicity of a bacterial secondary metabolite, namely, violacein, in Caenorhabditis elegans and found it is not only toxic towards adults, but also arrests growth and development of C. elegans larvae. To counteract this, C. elegans resorted to matriphagy, with the mothers holding their eggs within their bodies and hatching the young larvae internally, which eventually led to the mothers’ death. This violacein-induced matriphagy alleviated some of the toxic effects of violacein, allowing a portion of the internally-hatched young to bypass developmental arrest. Using genetic and pharmacological experiments, we found the consumption of oleate, a monounsaturated fatty acid produced by the mother, during matriphagy is partially responsible. As such, our study provides experimental evidence of why such a drastic and peculiar maternal behavior may have arisen in nematode natural habitats. Nature Publishing Group UK 2020-05-15 /pmc/articles/PMC7229185/ /pubmed/32415196 http://dx.doi.org/10.1038/s41598-020-64953-x Text en © The Author(s) 2020 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
Yoon, Kyoung-hye
Lee, Tong Young
Moon, Je-Hyun
Choi, Seong Yeol
Choi, Yun Ji
Mitchell, Robert J.
Il Lee, Jin
Consumption of Oleic Acid During Matriphagy in Free-Living Nematodes Alleviates the Toxic Effects of the Bacterial Metabolite Violacein
title Consumption of Oleic Acid During Matriphagy in Free-Living Nematodes Alleviates the Toxic Effects of the Bacterial Metabolite Violacein
title_full Consumption of Oleic Acid During Matriphagy in Free-Living Nematodes Alleviates the Toxic Effects of the Bacterial Metabolite Violacein
title_fullStr Consumption of Oleic Acid During Matriphagy in Free-Living Nematodes Alleviates the Toxic Effects of the Bacterial Metabolite Violacein
title_full_unstemmed Consumption of Oleic Acid During Matriphagy in Free-Living Nematodes Alleviates the Toxic Effects of the Bacterial Metabolite Violacein
title_short Consumption of Oleic Acid During Matriphagy in Free-Living Nematodes Alleviates the Toxic Effects of the Bacterial Metabolite Violacein
title_sort consumption of oleic acid during matriphagy in free-living nematodes alleviates the toxic effects of the bacterial metabolite violacein
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7229185/
https://www.ncbi.nlm.nih.gov/pubmed/32415196
http://dx.doi.org/10.1038/s41598-020-64953-x
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