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...
Published in: | Molecular Biology and Evolution |
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2022
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Online Access: | http://hdl.handle.net/10261/272884 https://doi.org/10.1093/molbev/msac096 https://doi.org/10.13039/501100000780 https://doi.org/10.13039/501100004837 https://doi.org/10.13039/501100005416 |
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ftcsic:oai:digital.csic.es:10261/272884 2024-02-11T09:58:31+01:00 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 Gil, Ana European Commission Ministerio de Ciencia e Innovación (España) Norwegian Research Council CSIC-UAM - Centro de Biología Molecular Severo Ochoa (CBM) 2022-05-05 http://hdl.handle.net/10261/272884 https://doi.org/10.1093/molbev/msac096 https://doi.org/10.13039/501100000780 https://doi.org/10.13039/501100004837 https://doi.org/10.13039/501100005416 en eng Oxford University Press #PLACEHOLDER_PARENT_METADATA_VALUE# info:eu-repo/grantAgreement/EC/H2020/841576 info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2019-105769GB-I00/ES/EVOLUCION DE LA REPRODUCCION SEXUAL ANIMAL: MAQUINARIA GENOMICA, MICROBIOMA Y PATRONES MACROEVOLUTIVOS EN ESPONJAS/ info:eu-repo/grantAgreement/MICINN//PID2020-117115GA-100 Publisher's version Sí Molecular Biology and Evolution 39(5): msac096 (2022) 0737-4038 http://hdl.handle.net/10261/272884 doi:10.1093/molbev/msac096 1537-1719 http://dx.doi.org/10.13039/501100000780 http://dx.doi.org/10.13039/501100004837 http://dx.doi.org/10.13039/501100005416 open Venom Toxins RNAseq Ribbon worm Mass spectrometry imaging Proteomics artículo 2022 ftcsic https://doi.org/10.1093/molbev/msac09610.13039/50110000078010.13039/50110000483710.13039/501100005416 2024-01-16T11:26:08Z 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 spectrom etry-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 sub due 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. This work was supported by the European Union’s Horizon 2020 Research and Innovation program through a Marie Sklodowska-Curie Individual Fellowship (grant agreement 841576), the Spanish Ministry of Science MCIN/AEI/10.13039/501100011033, European Union ... Article in Journal/Newspaper Antarc* Digital.CSIC (Spanish National Research Council) Molecular Biology and Evolution 39 5 |
institution |
Open Polar |
collection |
Digital.CSIC (Spanish National Research Council) |
op_collection_id |
ftcsic |
language |
English |
topic |
Venom Toxins RNAseq Ribbon worm Mass spectrometry imaging Proteomics |
spellingShingle |
Venom Toxins RNAseq Ribbon worm Mass spectrometry imaging Proteomics 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 Gil, Ana Evolution, Expression Patterns, and Distribution of Novel Ribbon Worm Predatory and Defensive Toxins |
topic_facet |
Venom Toxins RNAseq Ribbon worm Mass spectrometry imaging Proteomics |
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 spectrom etry-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 sub due 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. This work was supported by the European Union’s Horizon 2020 Research and Innovation program through a Marie Sklodowska-Curie Individual Fellowship (grant agreement 841576), the Spanish Ministry of Science MCIN/AEI/10.13039/501100011033, European Union ... |
author2 |
European Commission Ministerio de Ciencia e Innovación (España) Norwegian Research Council CSIC-UAM - Centro de Biología Molecular Severo Ochoa (CBM) |
format |
Article in Journal/Newspaper |
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 Gil, 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 Gil, 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://hdl.handle.net/10261/272884 https://doi.org/10.1093/molbev/msac096 https://doi.org/10.13039/501100000780 https://doi.org/10.13039/501100004837 https://doi.org/10.13039/501100005416 |
genre |
Antarc* |
genre_facet |
Antarc* |
op_relation |
#PLACEHOLDER_PARENT_METADATA_VALUE# info:eu-repo/grantAgreement/EC/H2020/841576 info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2019-105769GB-I00/ES/EVOLUCION DE LA REPRODUCCION SEXUAL ANIMAL: MAQUINARIA GENOMICA, MICROBIOMA Y PATRONES MACROEVOLUTIVOS EN ESPONJAS/ info:eu-repo/grantAgreement/MICINN//PID2020-117115GA-100 Publisher's version Sí Molecular Biology and Evolution 39(5): msac096 (2022) 0737-4038 http://hdl.handle.net/10261/272884 doi:10.1093/molbev/msac096 1537-1719 http://dx.doi.org/10.13039/501100000780 http://dx.doi.org/10.13039/501100004837 http://dx.doi.org/10.13039/501100005416 |
op_rights |
open |
op_doi |
https://doi.org/10.1093/molbev/msac09610.13039/50110000078010.13039/50110000483710.13039/501100005416 |
container_title |
Molecular Biology and Evolution |
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39 |
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5 |
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1790594193766219776 |