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

Research output: Contribution to journalArticlepeer-review

Ashlie Hartigan, Adrian Jaimes-Becerra, Beth Okamura, Liam B. Doonan, Malcolm Ward, Antonio C. Marques, Paul F. Long

Original languageEnglish
Article numbere11208
JournalPeerJ
Volume9
DOIs
Published26 Apr 2021

Bibliographical note

Funding Information: The following grant information was disclosed by the authors: Leverhulme Trust: RPG-2016-037. FAPESP: 2011/50242-5. CAPES: 88882.333070/2019-01 (236.507.518-52). CNPq: 309995/2017-5. Funding Information: Funding is from the Leverhulme Trust grant RPG-2016-037. Antonio C. Marques and Adrian Jaimes-Becerra received support from FAPESP (process 2011/50242-5) and CAPES (process 88882.333070/2019-01 [236.507.518-52]). Antonio C. Marques also received support from CNPq (process 309995/2017-5). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Publisher Copyright: Copyright 2021 Hartigan et al. Copyright: Copyright 2021 Elsevier B.V., All rights reserved.

King's Authors

Abstract

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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