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 Andreas Baste, Sonoda, Gabriel G., Andrade, Sonia C.S., Morato, Esperanza, Marina, Ana Isabel, Cárdenas, César A., Riesgo, Ana
Format: Article in Journal/Newspaper
Language:English
Published: 2022
Subjects:
Online Access:http://hdl.handle.net/10852/99885
https://doi.org/10.1093/molbev/msac096
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spelling ftoslouniv:oai:www.duo.uio.no:10852/99885 2023-05-15T13:38:06+02:00 Evolution, Expression Patterns, and Distribution of Novel Ribbon Worm Predatory and Defensive Toxins ENEngelskEnglishEvolution, Expression Patterns, and Distribution of Novel Ribbon Worm Predatory and Defensive Toxins Verdes, Aida Taboada, Sergi Hamilton, Brett R. Undheim, Eivind Andreas Baste Sonoda, Gabriel G. Andrade, Sonia C.S. Morato, Esperanza Marina, Ana Isabel Cárdenas, César A. Riesgo, Ana 2022-09-06T12:45:38Z http://hdl.handle.net/10852/99885 https://doi.org/10.1093/molbev/msac096 EN eng NFR/287462 EC/H2020/841576 EU/IJC2020-045256-I Verdes, Aida Taboada, Sergi Hamilton, Brett R. Undheim, Eivind Andreas Baste 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. Molecular Biology and Evolution (MBE). 2022, 39(5) http://hdl.handle.net/10852/99885 2049177 info:ofi/fmt:kev:mtx:ctx&ctx_ver=Z39.88-2004&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.jtitle=Molecular Biology and Evolution (MBE)&rft.volume=39&rft.spage=&rft.date=2022 Molecular Biology and Evolution (MBE) 39 5 16 https://doi.org/10.1093/molbev/msac096 Attribution 4.0 International https://creativecommons.org/licenses/by/4.0/ CC-BY 0737-4038 Journal article Tidsskriftartikkel Peer reviewed PublishedVersion 2022 ftoslouniv https://doi.org/10.1093/molbev/msac096 2023-02-15T23:36:38Z 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. Article in Journal/Newspaper Antarc* Universitet i Oslo: Digitale utgivelser ved UiO (DUO) Molecular Biology and Evolution 39 5
institution Open Polar
collection Universitet i Oslo: Digitale utgivelser ved UiO (DUO)
op_collection_id ftoslouniv
language English
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 Article in Journal/Newspaper
author Verdes, Aida
Taboada, Sergi
Hamilton, Brett R.
Undheim, Eivind Andreas Baste
Sonoda, Gabriel G.
Andrade, Sonia C.S.
Morato, Esperanza
Marina, Ana Isabel
Cárdenas, César A.
Riesgo, Ana
spellingShingle Verdes, Aida
Taboada, Sergi
Hamilton, Brett R.
Undheim, Eivind Andreas Baste
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
author_facet Verdes, Aida
Taboada, Sergi
Hamilton, Brett R.
Undheim, Eivind Andreas Baste
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
publishDate 2022
url http://hdl.handle.net/10852/99885
https://doi.org/10.1093/molbev/msac096
genre Antarc*
genre_facet Antarc*
op_source 0737-4038
op_relation NFR/287462
EC/H2020/841576
EU/IJC2020-045256-I
Verdes, Aida Taboada, Sergi Hamilton, Brett R. Undheim, Eivind Andreas Baste 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. Molecular Biology and Evolution (MBE). 2022, 39(5)
http://hdl.handle.net/10852/99885
2049177
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Molecular Biology and Evolution (MBE)
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https://doi.org/10.1093/molbev/msac096
op_rights Attribution 4.0 International
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