A Polychaete's powerful punch: venom gland transcriptomics of Glycera reveals a complex cocktail of toxin homologs

Genome Biol Evol. 2014 Sep 5;6(9):2406-23. doi: 10.1093/gbe/evu190.

Abstract

Glycerids are marine annelids commonly known as bloodworms. Bloodworms have an eversible proboscis adorned with jaws connected to venom glands. Bloodworms prey on invertebrates, and it is known that the venom glands produce compounds that can induce toxic effects in animals. Yet, none of these putative toxins has been characterized on a molecular basis. Here we present the transcriptomic profiles of the venom glands of three species of bloodworm, Glycera dibranchiata, Glycera fallax and Glycera tridactyla, as well as the body tissue of G. tridactyla. The venom glands express a complex mixture of transcripts coding for putative toxin precursors. These transcripts represent 20 known toxin classes that have been convergently recruited into animal venoms, as well as transcripts potentially coding for Glycera-specific toxins. The toxins represent five functional categories: Pore-forming and membrane-disrupting toxins, neurotoxins, protease inhibitors, other enzymes, and CAP domain toxins. Many of the transcripts coding for putative Glycera toxins belong to classes that have been widely recruited into venoms, but some are homologs of toxins previously only known from the venoms of scorpaeniform fish and monotremes (stonustoxin-like toxin), turrid gastropods (turripeptide-like peptides), and sea anemones (gigantoxin I-like neurotoxin). This complex mixture of toxin homologs suggests that bloodworms employ venom while predating on macroscopic prey, casting doubt on the previously widespread opinion that G. dibranchiata is a detritivore. Our results further show that researchers should be aware that different assembly methods, as well as different methods of homology prediction, can influence the transcriptomic profiling of venom glands.

Keywords: Annelida; Glycera; ShKT toxin; bloodworms; venom evolution; venomics.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Evolution, Molecular
  • Exocrine Glands / chemistry
  • Exocrine Glands / metabolism
  • Molecular Sequence Data
  • Phylogeny
  • Polychaeta / chemistry
  • Polychaeta / classification
  • Polychaeta / genetics*
  • Polychaeta / metabolism*
  • Sequence Alignment
  • Toxins, Biological / chemistry
  • Toxins, Biological / genetics*
  • Toxins, Biological / metabolism
  • Transcriptome
  • Venoms / chemistry
  • Venoms / genetics*
  • Venoms / metabolism

Substances

  • Toxins, Biological
  • Venoms

Associated data

  • GENBANK/GART00000000
  • GENBANK/GARU00000000
  • GENBANK/GARV00000000
  • GENBANK/GASB00000000