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, 13 (8), e0200944
eCollection

The Transcriptome of the Bermuda Fireworm Odontosyllis Enopla (Annelida: Syllidae): A Unique Luciferase Gene Family and Putative Epitoky-Related Genes

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The Transcriptome of the Bermuda Fireworm Odontosyllis Enopla (Annelida: Syllidae): A Unique Luciferase Gene Family and Putative Epitoky-Related Genes

Mercer R Brugler et al. PLoS One.

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.

Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Bioluminescent display of Odontosyllis enopla.
During the breeding period, female Odontosyllis enopla swim in slow circles secreting a bright bluish-green luminous mucus while releasing gametes. Photo credit: Dr. James B. Wood.
Fig 2
Fig 2. Multiple sequence alignment of the Odontosyllis enopla luciferase gene with that of the Japanese syllid O. undecimdonta.
The Odontosyllis enopla luciferase gene (329 amino acids in length) is aligned with the four putative luciferase transcripts (isoforms) of O. undecimdonta. The alignment was generated using default parameters and the L-INS-i iterative refinement method within MAFFT (v7.402). Ou: O. undecimdonta. Oe1: O. enopla Individual 1.
Fig 3
Fig 3. An unrooted maximum likelihood-based phylogenetic tree showing the relationship of both orthologs and paralogs of the luciferase gene for Odontosyllis enopla and O. undecimdonta.
The four transcripts (isoforms) found by Schultz et al. [44] are in orange. ‘O_undecimdonta_DN31989’ (green) is identical to one of the four isoforms but has a different name because it is based on our Trinity assembly. The two additional green terminals are paralogs of the O. undecimdonta luciferase that were not reported by Schultz et al. [44]. For O. enopla, orthologs are shown in purple and the paralogs in blue. O_enopla_1: Individual 1, O_enopla_2: Individual 2, O_enopla_3: Individual 3. The ML tree was constructed using a MUSCLE-based amino acid alignment and the following parameters: WAG + gamma + I model; aLRT-based support values.

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Grant support

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.
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