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Recruitment of toxin-like proteins with ancestral venom function supports endoparasitic lifestyles of Myxozoa

Cnidarians are the oldest lineage of venomous animals and use nematocysts to discharge toxins. Whether venom toxins have been recruited to support parasitic lifestyles in the Endocnidozoa (Myxozoa + Polypodium) is, however, unknown. To examine this issue we variously employed transcriptomic, proteom...

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Autores principales: Hartigan, Ashlie, Jaimes-Becerra, Adrian, Okamura, Beth, Doonan, Liam B., Ward, Malcolm, Marques, Antonio C., Long, Paul F.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: PeerJ Inc. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8083181/
https://www.ncbi.nlm.nih.gov/pubmed/33981497
http://dx.doi.org/10.7717/peerj.11208
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author Hartigan, Ashlie
Jaimes-Becerra, Adrian
Okamura, Beth
Doonan, Liam B.
Ward, Malcolm
Marques, Antonio C.
Long, Paul F.
author_facet Hartigan, Ashlie
Jaimes-Becerra, Adrian
Okamura, Beth
Doonan, Liam B.
Ward, Malcolm
Marques, Antonio C.
Long, Paul F.
author_sort Hartigan, Ashlie
collection PubMed
description Cnidarians are the oldest lineage of venomous animals and use nematocysts to discharge toxins. Whether venom toxins have been recruited to support parasitic lifestyles in the Endocnidozoa (Myxozoa + Polypodium) is, however, unknown. To examine this issue we variously employed transcriptomic, proteomic, associated molecular phylogenies, and localisation studies on representative primitive and derived myxozoans (Malacosporea and Myxosporea, respectively), Polypodium hydriforme, and the free-living staurozoan Calvadosia cruxmelitensis. Our transcriptomics and proteomics analyses provide evidence for expression and translation of venom toxin homologs in myxozoans. Phylogenetic placement of Kunitz type serine protease inhibitors and phospholipase A2 enzymes reveals modification of toxins inherited from ancestral free-living cnidarian toxins, and that venom diversity is reduced in myxozoans concordant with their reduced genome sizes. Various phylogenetic analyses of the Kunitz-type toxin family in Endocnidozoa suggested lineage-specific gene duplications, which offers a possible mechanism for enhancing toxin diversification. Toxin localisation in the malacosporean Buddenbrockia plumatellae substantiates toxin translation and thus illustrates a repurposing of toxin function for endoparasite development and interactions with hosts, rather than for prey capture or defence. Whether myxozoan venom candidates are expressed in transmission stages (e.g. in nematocysts or secretory vesicles) requires further investigation.
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spelling pubmed-80831812021-05-11 Recruitment of toxin-like proteins with ancestral venom function supports endoparasitic lifestyles of Myxozoa Hartigan, Ashlie Jaimes-Becerra, Adrian Okamura, Beth Doonan, Liam B. Ward, Malcolm Marques, Antonio C. Long, Paul F. PeerJ Environmental Sciences Cnidarians are the oldest lineage of venomous animals and use nematocysts to discharge toxins. Whether venom toxins have been recruited to support parasitic lifestyles in the Endocnidozoa (Myxozoa + Polypodium) is, however, unknown. To examine this issue we variously employed transcriptomic, proteomic, associated molecular phylogenies, and localisation studies on representative primitive and derived myxozoans (Malacosporea and Myxosporea, respectively), Polypodium hydriforme, and the free-living staurozoan Calvadosia cruxmelitensis. Our transcriptomics and proteomics analyses provide evidence for expression and translation of venom toxin homologs in myxozoans. Phylogenetic placement of Kunitz type serine protease inhibitors and phospholipase A2 enzymes reveals modification of toxins inherited from ancestral free-living cnidarian toxins, and that venom diversity is reduced in myxozoans concordant with their reduced genome sizes. Various phylogenetic analyses of the Kunitz-type toxin family in Endocnidozoa suggested lineage-specific gene duplications, which offers a possible mechanism for enhancing toxin diversification. Toxin localisation in the malacosporean Buddenbrockia plumatellae substantiates toxin translation and thus illustrates a repurposing of toxin function for endoparasite development and interactions with hosts, rather than for prey capture or defence. Whether myxozoan venom candidates are expressed in transmission stages (e.g. in nematocysts or secretory vesicles) requires further investigation. PeerJ Inc. 2021-04-26 /pmc/articles/PMC8083181/ /pubmed/33981497 http://dx.doi.org/10.7717/peerj.11208 Text en © 2021 Hartigan et al. 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 use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ) and either DOI or URL of the article must be cited.
spellingShingle Environmental Sciences
Hartigan, Ashlie
Jaimes-Becerra, Adrian
Okamura, Beth
Doonan, Liam B.
Ward, Malcolm
Marques, Antonio C.
Long, Paul F.
Recruitment of toxin-like proteins with ancestral venom function supports endoparasitic lifestyles of Myxozoa
title Recruitment of toxin-like proteins with ancestral venom function supports endoparasitic lifestyles of Myxozoa
title_full Recruitment of toxin-like proteins with ancestral venom function supports endoparasitic lifestyles of Myxozoa
title_fullStr Recruitment of toxin-like proteins with ancestral venom function supports endoparasitic lifestyles of Myxozoa
title_full_unstemmed Recruitment of toxin-like proteins with ancestral venom function supports endoparasitic lifestyles of Myxozoa
title_short Recruitment of toxin-like proteins with ancestral venom function supports endoparasitic lifestyles of Myxozoa
title_sort recruitment of toxin-like proteins with ancestral venom function supports endoparasitic lifestyles of myxozoa
topic Environmental Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8083181/
https://www.ncbi.nlm.nih.gov/pubmed/33981497
http://dx.doi.org/10.7717/peerj.11208
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