Evolution, Expression Patterns, and Distribution of Novel Ribbon Worm Predatory and Defensive Toxins

Ribbon worms are active predators that use an eversible proboscis to inject venom into their prey and defend themselves with toxic epidermal secretions. Previous work on nemertean venom has largely focused on just a few species and has not investigated the different predatory and defensive secretion...

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Published in:Molecular Biology and Evolution
Main Authors: Verdes, Aida, Taboada, Sergi, Hamilton, Brett R., Undheim, Eivind A.B., Sonoda, Gabriel G., Andrade, Sonia C.S., Morato, Esperanza, Marina, Ana Isabel, Cárdenas, César A., Riesgo, Ana
Format: Text
Language:English
Published: Oxford University Press 2022
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Online Access:http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9132205/
http://www.ncbi.nlm.nih.gov/pubmed/35512366
https://doi.org/10.1093/molbev/msac096
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spelling ftpubmed:oai:pubmedcentral.nih.gov:9132205 2023-05-15T14:01:33+02:00 Evolution, Expression Patterns, and Distribution of Novel Ribbon Worm Predatory and Defensive Toxins Verdes, Aida Taboada, Sergi Hamilton, Brett R. Undheim, Eivind A.B. Sonoda, Gabriel G. Andrade, Sonia C.S. Morato, Esperanza Marina, Ana Isabel Cárdenas, César A. Riesgo, Ana 2022-05-05 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9132205/ http://www.ncbi.nlm.nih.gov/pubmed/35512366 https://doi.org/10.1093/molbev/msac096 en eng Oxford University Press http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9132205/ http://www.ncbi.nlm.nih.gov/pubmed/35512366 http://dx.doi.org/10.1093/molbev/msac096 © The Author(s) 2022. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. CC-BY Mol Biol Evol Discoveries Text 2022 ftpubmed https://doi.org/10.1093/molbev/msac096 2022-05-29T00:51:00Z Ribbon worms are active predators that use an eversible proboscis to inject venom into their prey and defend themselves with toxic epidermal secretions. Previous work on nemertean venom has largely focused on just a few species and has not investigated the different predatory and defensive secretions in detail. Consequently, our understanding of the composition and evolution of ribbon worm venoms is still very limited. Here, we present a comparative study of nemertean venom combining RNA-seq differential gene expression analyses of venom-producing tissues, tandem mass spectrometry-based proteomics of toxic secretions, and mass spectrometry imaging of proboscis sections, to shed light onto the composition and evolution of predatory and defensive toxic secretions in Antarctonemertes valida. Our analyses reveal a wide diversity of putative defensive and predatory toxins with tissue-specific gene expression patterns and restricted distributions to the mucus and proboscis proteomes respectively, suggesting that ribbon worms produce distinct toxin cocktails for predation and defense. Our results also highlight the presence of numerous lineage-specific toxins, indicating that venom evolution is highly divergent across nemerteans, producing toxin cocktails that might be finely tuned to subdue different prey. Our data also suggest that the hoplonemertean proboscis is a highly specialized predatory organ that seems to be involved in a variety of biological functions besides predation, including secretion and sensory perception. Overall, our results advance our knowledge into the diversity and evolution of nemertean venoms and highlight the importance of combining different types of data to characterize toxin composition in understudied venomous organisms. Text Antarc* PubMed Central (PMC) Molecular Biology and Evolution 39 5
institution Open Polar
collection PubMed Central (PMC)
op_collection_id ftpubmed
language English
topic Discoveries
spellingShingle Discoveries
Verdes, Aida
Taboada, Sergi
Hamilton, Brett R.
Undheim, Eivind A.B.
Sonoda, Gabriel G.
Andrade, Sonia C.S.
Morato, Esperanza
Marina, Ana Isabel
Cárdenas, César A.
Riesgo, Ana
Evolution, Expression Patterns, and Distribution of Novel Ribbon Worm Predatory and Defensive Toxins
topic_facet Discoveries
description Ribbon worms are active predators that use an eversible proboscis to inject venom into their prey and defend themselves with toxic epidermal secretions. Previous work on nemertean venom has largely focused on just a few species and has not investigated the different predatory and defensive secretions in detail. Consequently, our understanding of the composition and evolution of ribbon worm venoms is still very limited. Here, we present a comparative study of nemertean venom combining RNA-seq differential gene expression analyses of venom-producing tissues, tandem mass spectrometry-based proteomics of toxic secretions, and mass spectrometry imaging of proboscis sections, to shed light onto the composition and evolution of predatory and defensive toxic secretions in Antarctonemertes valida. Our analyses reveal a wide diversity of putative defensive and predatory toxins with tissue-specific gene expression patterns and restricted distributions to the mucus and proboscis proteomes respectively, suggesting that ribbon worms produce distinct toxin cocktails for predation and defense. Our results also highlight the presence of numerous lineage-specific toxins, indicating that venom evolution is highly divergent across nemerteans, producing toxin cocktails that might be finely tuned to subdue different prey. Our data also suggest that the hoplonemertean proboscis is a highly specialized predatory organ that seems to be involved in a variety of biological functions besides predation, including secretion and sensory perception. Overall, our results advance our knowledge into the diversity and evolution of nemertean venoms and highlight the importance of combining different types of data to characterize toxin composition in understudied venomous organisms.
format Text
author Verdes, Aida
Taboada, Sergi
Hamilton, Brett R.
Undheim, Eivind A.B.
Sonoda, Gabriel G.
Andrade, Sonia C.S.
Morato, Esperanza
Marina, Ana Isabel
Cárdenas, César A.
Riesgo, Ana
author_facet Verdes, Aida
Taboada, Sergi
Hamilton, Brett R.
Undheim, Eivind A.B.
Sonoda, Gabriel G.
Andrade, Sonia C.S.
Morato, Esperanza
Marina, Ana Isabel
Cárdenas, César A.
Riesgo, Ana
author_sort Verdes, Aida
title Evolution, Expression Patterns, and Distribution of Novel Ribbon Worm Predatory and Defensive Toxins
title_short Evolution, Expression Patterns, and Distribution of Novel Ribbon Worm Predatory and Defensive Toxins
title_full Evolution, Expression Patterns, and Distribution of Novel Ribbon Worm Predatory and Defensive Toxins
title_fullStr Evolution, Expression Patterns, and Distribution of Novel Ribbon Worm Predatory and Defensive Toxins
title_full_unstemmed Evolution, Expression Patterns, and Distribution of Novel Ribbon Worm Predatory and Defensive Toxins
title_sort evolution, expression patterns, and distribution of novel ribbon worm predatory and defensive toxins
publisher Oxford University Press
publishDate 2022
url http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9132205/
http://www.ncbi.nlm.nih.gov/pubmed/35512366
https://doi.org/10.1093/molbev/msac096
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op_source Mol Biol Evol
op_relation http://www.ncbi.nlm.nih.gov/pmc/articles/PMC9132205/
http://www.ncbi.nlm.nih.gov/pubmed/35512366
http://dx.doi.org/10.1093/molbev/msac096
op_rights © The Author(s) 2022. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution.
https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
op_rightsnorm CC-BY
op_doi https://doi.org/10.1093/molbev/msac096
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