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Sci Rep
2020 Oct 20;101:17724. doi: 10.1038/s41598-020-73446-w.
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A putative chordate luciferase from a cosmopolitan tunicate indicates convergent bioluminescence evolution across phyla.
Tessler M
,
Gaffney JP
,
Oliveira AG
,
Guarnaccia A
,
Dobi KC
,
Gujarati NA
,
Galbraith M
,
Mirza JD
,
Sparks JS
,
Pieribone VA
,
Wood RJ
,
Gruber DF
.
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Pyrosomes are tunicates in the phylum Chordata, which also contains vertebrates. Their gigantic blooms play important ecological and biogeochemical roles in oceans. Pyrosoma, meaning "fire-body", derives from their brilliant bioluminescence. The biochemistry of this light production is unknown, but has been hypothesized to be bacterial in origin. We found that mixing coelenterazine-a eukaryote-specific luciferin-with Pyrosoma atlanticum homogenate produced light. To identify the bioluminescent machinery, we sequenced P. atlanticum transcriptomes and found a sequence match to a cnidarian luciferase (RLuc). We expressed this novel luciferase (PyroLuc) and, combined with coelenterazine, it produced light. A similar gene was recently predicted from a bioluminescent brittle star, indicating that RLuc-like luciferases may have evolved convergently from homologous dehalogenases across phyla (Cnidaria, Echinodermata, and Chordata). This report indicates that a widespread gene may be able to functionally converge, resulting in bioluminescence across animal phyla, and describes and characterizes the first putative chordate luciferase.
Figure 1. Pyrosomes—Pyrosoma atlanticum (A,B; ~ 155 mm × 40 mm) and Pyrosomella verticillata (C,D; ~ 25 mm × 40 mm)—from SE Brazilian Atlantic under (A,C) white light and (B,D) producing bioluminescence following mechanical stimulation; (E) soft robotic arm collection of Pyrosoma atlanticum from the NE Brazilian Atlantic from Nadir (Triton 3300/3 submarine).
Figure 2. (A) Predicted model of PyroLuc created using SWISS-Model based on Renilla luciferase and (B) model of Renilla luciferase (2PSJ33). Both models were rendered in PyMOL 2.3 (https://pymol.org). Magenta sticks show conserved active site residues in the coelenterazine binding site. (C) Alignment of PyroLuc and RLuc. The residues highlighted in blue make up the catalytic triad in RLuc and those in red represent those in the coelenterazine binding site. Bold type represents identical residues.
Figure 3. In blue, luminescence reading of purified PyroLuc (3.2 μM) following the addition of coelenterazine (24.5 μM). PyroLuc and coelenterazine were diluted in PBS with 300 mM imidazole, pH 7.4. In green, PBS buffer control with addition of 24.54 μM coelenterazine. Coelenterazine was injected at 16 s for both experiments.
Figure 4. Maximum likelihood phylogeny of RLuc-like luciferases (bolded) and haloalkane dehalogenases. PyroLuc from Pyrosoma atlanticum is accentuated with a box. Support values are summaries of 1000 bootstrap replicates. The luciferases from A. filiformis have yet to be functionally confirmed, but are highly probable29.
Figure 5. Expression of Renilla-like luciferase protein in Pyrosoma atlanticum. (A–F) Extended focus confocal projections of pyrosomes immunostained with an antibody to Renilla luciferase (anti-RLuc, green) and Hoechst (blue) to label nuclei. External views show incurrent siphons (s) of multiple (A–C) or single (D–F) zooids. Greyscale shown for A, B, D, and E; fluorescence shown for C and F. RLuc-like protein immunolocalizes to a large, circular structure underlying the incurrent siphon (A, arrowhead). (G–H) Fluorescent stereomicroscope images of a sample incubated with RLuc antibody (G) or rabbit pre-immune serum as a control (H). Individual patches of staining outside the siphon (arrows) appear to be localized to the tunic, and were shown to be non-specific using pre-immune serum (G, H and data not shown). Internal circular staining is specific to the RLuc antibody (G, arrowhead). Scale bars, 500 μm.
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