The transcriptome of the Bermuda fireworm Odontosyllis enopla (Annelida: Syllidae): A unique luciferase gene family and putative epitoky-related genes

PLoS One. 2018 Aug 8;13(8):e0200944. doi: 10.1371/journal.pone.0200944. eCollection 2018.

Abstract

The Bermuda fireworm Odontosyllis enopla exhibits an extremely tight circalunar circadian behavior that results in an impressive bioluminescent mating swarm, thought to be due to a conventional luciferase-mediated oxidation of a light-emitting luciferin. In addition, the four eyes become hypertrophied and heavily pigmented, and the nephridial system is modified to store and release gametes and associated secretions. In an effort to elucidate transcripts related to bioluminescence, circadian or circalunar periodicity, as well as epitoky-related changes of the eyes and nephridial system, we examined the transcriptomic profile of three female O. enopla during a bioluminescent swarm in Ferry Reach, Bermuda. Using the well-characterized luciferase gene of the Japanese syllid Odontosyllis undecimdonta as a reference, a complete best-matching luciferase open reading frame (329 amino acids in length) was found in all three individuals analyzed in addition to numerous other paralogous sequences in this new gene family. No photoproteins were detected. We also recovered a predicted homolog of 4-coumarate-CoA ligase (268 amino acids in length) that best matched luciferase of the firefly Luciola with the best predicted template being the crystal structure of luciferase for Photinus pyralis, the common eastern firefly. A wide variety of genes associated with periodicity were recovered including predicted homologs of clock, bmal1, period, and timeless. Several genes corresponding to putative epitoky-related changes of the eyes were recovered including predicted homologs of a phototransduction gene, a retinol dehydrogenase and carotenoid isomerooxygenase as well as a visual perception related retinal rod rhodopsin-sensitive cGMP 3',5'-cyclic phosphodiesterase. Genes correlating to putative epitoky-related changes of the nephridia included predicted homologs of nephrocystin-3 and an egg-release sex peptide receptor.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Annelida / genetics*
  • Circadian Rhythm / genetics
  • Fireflies / metabolism
  • Luciferases / genetics*
  • Luciferases, Firefly / genetics
  • Luminescent Measurements
  • Phylogeny
  • Polychaeta / metabolism
  • Sexual Maturation
  • Transcriptome

Substances

  • Luciferases
  • Luciferases, Firefly

Grants and funding

The Gerstner Family Foundation provided partial support to MRB. MTA received support as the PI of the project “Macroevolutionary transitions in Syllidae” CGL2015-63593-P from MINECO/FEDER, UE funds. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. There was no additional external funding received for this study.