A phylogeny-aware approach reveals unexpected venom components in divergent lineages of cone snails

Type Article
Date 2021-07
Language English
Author(s) Fedosov AlexanderORCID1, 2, Zaharias PaulORCID2, 3, Puillandre NicolasORCID2
Affiliation(s) 1 : A.N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Leninsky Prospect 33, 119071 Moscow, Russian Federation
2 : Institut Systématique Evolution Biodiversité (ISYEB), Muséum National d'Histoire Naturelle, CNRS, Sorbonne Université, EPHE, Université des Antilles, 57 rue Cuvier, CP 26, 75005 Paris, France
3 : Department of Computer Science, University of Illinois Urbana-Champaign, Urbana, IL 61801, USA
Source Proceedings of the Royal Society B: Biological Sciences (0962-8452) (The Royal Society), 2021-07 , Vol. 288 , N. 1954 , P. 20211017 (9p.)
DOI 10.1098/rspb.2021.1017
Keyword(s) conotoxins, venom evolution, phylogeny, Conidae, Conasprella, Pygmaeconus

Marine gastropods of the genus Conus are renowned for their remarkable diversity and deadly venoms. While Conus venoms are increasingly well studied for their biomedical applications, we know surprisingly little about venom composition in other lineages of Conidae. We performed comprehensive venom transcriptomic profiling for Conasprella coriolisi and Pygmaeconus traillii, first time for both respective genera. We complemented reference-based transcriptome annotation by a de novo toxin prediction guided by phylogeny, which involved transcriptomic data on two additional ‘divergent’ cone snail lineages, Profundiconus, and Californiconus. We identified toxin clusters (SSCs) shared among all or some of the four analysed genera based on the identity of the signal region—a molecular tag present in toxins. In total, 116 and 98 putative toxins represent 29 and 28 toxin gene superfamilies in Conasprella and Pygmaeconus, respectively; about quarter of these only found by semi-manual annotation of the SSCs. Two rare gene superfamilies, originally identified from fish-hunting cone snails, were detected outside Conus rather unexpectedly, so we further investigated their distribution across Conidae radiation. We demonstrate that both these, in fact, are ubiquitous in Conidae, sometimes with extremely high expression. Our findings demonstrate how a phylogeny-aware approach circumvents methodological caveats of similarity-based transcriptome annotation.

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