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Acquired stress resilience through bacteria-to-nematode horizontal gene transfer
Natural selection drives acquisition of organismal resilience traits to protect against adverse environments. Horizontal gene transfer (HGT) is an important evolutionary mechanism for the acquisition of novel traits, including metazoan acquisition of functions in immunity, metabolism, and reproducti...
Autores principales: | , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Cold Spring Harbor Laboratory
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10473587/ https://www.ncbi.nlm.nih.gov/pubmed/37662235 http://dx.doi.org/10.1101/2023.08.20.554039 |
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author | Pandey, Taruna Kalluraya, Chinmay Wang, Bingying Xu, Ting Huang, Xinya Guang, Shouhong Daugherty, Matthew D. Ma, Dengke K. |
author_facet | Pandey, Taruna Kalluraya, Chinmay Wang, Bingying Xu, Ting Huang, Xinya Guang, Shouhong Daugherty, Matthew D. Ma, Dengke K. |
author_sort | Pandey, Taruna |
collection | PubMed |
description | Natural selection drives acquisition of organismal resilience traits to protect against adverse environments. Horizontal gene transfer (HGT) is an important evolutionary mechanism for the acquisition of novel traits, including metazoan acquisition of functions in immunity, metabolism, and reproduction via interdomain HGT (iHGT) from bacteria. We report that the nematode gene rml-3, which was acquired by iHGT from bacteria, enables exoskeleton resilience and protection against environmental toxins in C. elegans. Phylogenetic analysis reveals that diverse nematode RML-3 proteins form a single monophyletic clade most highly similar to bacterial enzymes that biosynthesize L-rhamnose to build cell wall polysaccharides. C. elegans rml-3 is regulated in developing seam cells by heat stress and stress-resistant dauer stage. Importantly, rml-3 deficiency impairs cuticle integrity, barrier functions and organismal stress resilience, phenotypes that are rescued by exogenous L-rhamnose. We propose that iHGT of an ancient bacterial rml-3 homolog enables L-rhamnose biosynthesis in nematodes that facilitates cuticle integrity and organismal resilience in adaptation to environmental stresses during evolution. These findings highlight the remarkable contribution of iHGT on metazoan evolution that is conferred by the domestication of bacterial genes. |
format | Online Article Text |
id | pubmed-10473587 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | Cold Spring Harbor Laboratory |
record_format | MEDLINE/PubMed |
spelling | pubmed-104735872023-09-02 Acquired stress resilience through bacteria-to-nematode horizontal gene transfer Pandey, Taruna Kalluraya, Chinmay Wang, Bingying Xu, Ting Huang, Xinya Guang, Shouhong Daugherty, Matthew D. Ma, Dengke K. bioRxiv Article Natural selection drives acquisition of organismal resilience traits to protect against adverse environments. Horizontal gene transfer (HGT) is an important evolutionary mechanism for the acquisition of novel traits, including metazoan acquisition of functions in immunity, metabolism, and reproduction via interdomain HGT (iHGT) from bacteria. We report that the nematode gene rml-3, which was acquired by iHGT from bacteria, enables exoskeleton resilience and protection against environmental toxins in C. elegans. Phylogenetic analysis reveals that diverse nematode RML-3 proteins form a single monophyletic clade most highly similar to bacterial enzymes that biosynthesize L-rhamnose to build cell wall polysaccharides. C. elegans rml-3 is regulated in developing seam cells by heat stress and stress-resistant dauer stage. Importantly, rml-3 deficiency impairs cuticle integrity, barrier functions and organismal stress resilience, phenotypes that are rescued by exogenous L-rhamnose. We propose that iHGT of an ancient bacterial rml-3 homolog enables L-rhamnose biosynthesis in nematodes that facilitates cuticle integrity and organismal resilience in adaptation to environmental stresses during evolution. These findings highlight the remarkable contribution of iHGT on metazoan evolution that is conferred by the domestication of bacterial genes. Cold Spring Harbor Laboratory 2023-08-21 /pmc/articles/PMC10473587/ /pubmed/37662235 http://dx.doi.org/10.1101/2023.08.20.554039 Text en https://creativecommons.org/licenses/by-nc-nd/4.0/This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (https://creativecommons.org/licenses/by-nc-nd/4.0/) , which allows reusers to copy and distribute the material in any medium or format in unadapted form only, for noncommercial purposes only, and only so long as attribution is given to the creator. |
spellingShingle | Article Pandey, Taruna Kalluraya, Chinmay Wang, Bingying Xu, Ting Huang, Xinya Guang, Shouhong Daugherty, Matthew D. Ma, Dengke K. Acquired stress resilience through bacteria-to-nematode horizontal gene transfer |
title | Acquired stress resilience through bacteria-to-nematode horizontal gene transfer |
title_full | Acquired stress resilience through bacteria-to-nematode horizontal gene transfer |
title_fullStr | Acquired stress resilience through bacteria-to-nematode horizontal gene transfer |
title_full_unstemmed | Acquired stress resilience through bacteria-to-nematode horizontal gene transfer |
title_short | Acquired stress resilience through bacteria-to-nematode horizontal gene transfer |
title_sort | acquired stress resilience through bacteria-to-nematode horizontal gene transfer |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10473587/ https://www.ncbi.nlm.nih.gov/pubmed/37662235 http://dx.doi.org/10.1101/2023.08.20.554039 |
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