Transcriptomic Profiling Reveals Extraordinary Diversity of Venom Peptides in Unexplored Predatory Gastropods of the Genus Clavus

Author:

Lu Aiping1ORCID,Watkins Maren2,Li Qing34,Robinson Samuel D2,Concepcion Gisela P5,Yandell Mark36,Weng Zhiping17,Olivera Baldomero M2,Safavi-Hemami Helena89,Fedosov Alexander E10ORCID

Affiliation:

1. Department of Central Laboratory, Shanghai Tenth People’s Hospital of Tongji University, School of Life Sciences and Technology, Tongji University, Shanghai, China

2. Department of Biology, University of Utah

3. Eccles Institute of Human Genetics, University of Utah

4. High-Throughput Genomics and Bioinformatic Analysis Shared Resource, Huntsman Cancer Institute, University of Utah

5. Marine Science Institute, University of the Philippines-Diliman, Quezon City, Philippines

6. Utah Center for Genetic Discovery, University of Utah

7. Program in Bioinformatics and Integrative Biology, University of Massachusetts Medical School

8. Department of Biochemistry, University of Utah

9. Department of Biology, University of Copenhagen, Denmark

10. A.N. Severtsov Institute of Ecology and Evolution, Russian Academy of Science, Moscow, Russia

Abstract

Abstract Predatory gastropods of the superfamily Conoidea number over 12,000 living species. The evolutionary success of this lineage can be explained by the ability of conoideans to produce complex venoms for hunting, defense, and competitive interactions. Whereas venoms of cone snails (family Conidae) have become increasingly well studied, the venoms of most other conoidean lineages remain largely uncharacterized. In the present study, we present the venom gland transcriptomes of two species of the genus Clavus that belong to the family Drilliidae. Venom gland transcriptomes of two specimens of Clavus canalicularis and two specimens of Clavus davidgilmouri were analyzed, leading to the identification of a total of 1,176 putative venom peptide toxins (drillipeptides). Based on the combined evidence of secretion signal sequence identity, entire precursor similarity search (BLAST), and the orthology inference, putative Clavus toxins were assigned to 158 different gene families. The majority of identified transcripts comprise signal, pro-, mature peptide, and post-regions, with a typically short (<50 amino acids) and cysteine-rich mature peptide region. Thus, drillipeptides are structurally similar to conotoxins. However, convincing homology with known groups of Conus toxins was only detected for very few toxin families. Among these are Clavus counterparts of Conus venom insulins (drillinsulins), porins (drilliporins), and highly diversified lectins (drillilectins). The short size of most drillipeptides and structural similarity to conotoxins were unexpected, given that most related conoidean gastropod families (Terebridae and Turridae) possess longer mature peptide regions. Our findings indicate that, similar to conotoxins, drillipeptides may represent a valuable resource for future pharmacological exploration.

Funder

National Institutes of Health

Villum Young Investigator

National Natural Science Foundation of China

Shanghai Natural Science Foundation of China

Russian Science Foundation

Publisher

Oxford University Press (OUP)

Subject

Genetics,Ecology, Evolution, Behavior and Systematics

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