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Luciferin Production and Luciferase Transcription in the Bioluminescent Copepod Metridia lucens

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Luciferin Production and Luciferase Transcription in the Bioluminescent Copepod Metridia lucens

Michael Tessler et al. PeerJ.

Abstract

Bioluminescent copepods are often the most abundant marine zooplankton and play critical roles in oceanic food webs. Metridia copepods exhibit particularly bright bioluminescence, and the molecular basis of their light production has just recently begun to be explored. Here we add to this body of work by transcriptomically profiling Metridia lucens, a common species found in temperate, northern, and southern latitudes. In this previously molecularly-uncharacterized species, we find the typical luciferase paralog gene set found in Metridia. More surprisingly, we recover noteworthy putative luciferase sequences that had not been described from Metridia species, indicating that bioluminescence produced by these copepods may be more complex than previously known. This includes another copepod luciferase, as well as one from a shrimp. Furthermore, feeding experiments using mass spectrometry and 13C labelled L-tyrosine and L-phenylalanine firmly establish that M. lucens produces its own coelenterazine luciferin rather than acquiring it through diet. This coelenterazine synthesis has only been directly confirmed in one other copepod species.

Keywords: Coelenteramine; Coelenterazine; Copepoda; Luciferase; Luciferin; Metridia lucens.

Conflict of interest statement

The authors declare there are no competing interests.

Figures

Figure 1
Figure 1. Light microscopy of Metridia lucens.
Under normal light (A) and while excreting bioluminesce (B).
Figure 2
Figure 2. Maximum likelihood phylogenetic reconstruction of luciferases from Metridia species and related copepods.
Support values are summaries of 1,000 bootstrap replicates. Image credit for copepod drawing: Olivia A. Gresham.
Figure 3
Figure 3. Maximum likelihood phylogeny of COI of Metridia copepods.
Support values are summaries of 1,000 bootstrap replicates. * The North Atlantic Metridia lucens clade contains the COI sequence from our M. lucens transcriptome. 1In addition to the Pleuromamma species, a sequence of Metridia venusta was also found in this clade.
Figure 4
Figure 4. EIC analysis of the labeled coelenteramines.
(A) Extracted ion count chromatograms (EICs, extraction window ±10 ppm) for natural 12C-coelenteramine (M + H) under 13C-labeling and non-labeling conditions. (B/C) EICs for the 13C9-labeled (B) and the 13C8-labeled (C) coelenteramine ions centered at m/z 287.1590 and m/z 286.1556 are shown. Data support that the carbons depicted in red are isotopically labeled at low abundance. The peak at 14.4 min has the same retention time as the coelenteramine standard. Observed for 13C8-coelenteramine: 286.1561, 1.7 ppm error. Observed for 13C9-coelenteramine: 287.1598, 2.8 ppm error.

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Grant support

This work was supported by DARPA-NESD Grant #N66001-17-C-4012 to Vincent A. Pieribone, David F. Gruber, Jean P. Gaffney, Jason M. Crawford. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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