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Open Access Highly Accessed Research article

Genomic organization, evolution, and expression of photoprotein and opsin genes in Mnemiopsis leidyi: a new view of ctenophore photocytes

Christine E Schnitzler1, Kevin Pang2, Meghan L Powers3, Adam M Reitzel4, Joseph F Ryan2, David Simmons5, Takashi Tada6, Morgan Park7, Jyoti Gupta7, Shelise Y Brooks7, Robert W Blakesley17, Shozo Yokoyama6, Steven HD Haddock3, Mark Q Martindale5 and Andreas D Baxevanis1*

Author affiliations

1 Genome Technology Branch, Division of Intramural Research, National Human Genome Research Institute, National Institutes of Health, 50 South Drive, Bethesda, MD 20892, USA

2 Sars International Centre for Marine Molecular Biology, Thormøhlensgt. 55, N-5008, Bergen Norway

3 Monterey Bay Aquarium Research Institute, 7700 Sandholdt Road, Moss Landing, CA 95039, USA

4 Department of Biology, University of North Carolina at Charlotte, 9210 University City Boulevard, Charlotte, NC 28223, USA

5 Kewalo Marine Laboratory, Pacific Biosciences Research Center, University of Hawaii at Manoa, 41 Ahui Street, Honolulu, HI 96813, USA

6 Department of Biology, Emory University, 1510 Clifton Road NE, Atlanta, GA 30322, USA

7 NIH Intramural Sequencing Center, National Human Genome Research Institute, National Institutes of Health, 5625 Fishers Lane, Rockville, MD 20852, USA

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Citation and License

BMC Biology 2012, 10:107  doi:10.1186/1741-7007-10-107

Published: 21 December 2012

Abstract

Background

Calcium-activated photoproteins are luciferase variants found in photocyte cells of bioluminescent jellyfish (Phylum Cnidaria) and comb jellies (Phylum Ctenophora). The complete genomic sequence from the ctenophore Mnemiopsis leidyi, a representative of the earliest branch of animals that emit light, provided an opportunity to examine the genome of an organism that uses this class of luciferase for bioluminescence and to look for genes involved in light reception. To determine when photoprotein genes first arose, we examined the genomic sequence from other early-branching taxa. We combined our genomic survey with gene trees, developmental expression patterns, and functional protein assays of photoproteins and opsins to provide a comprehensive view of light production and light reception in Mnemiopsis.

Results

The Mnemiopsis genome has 10 full-length photoprotein genes situated within two genomic clusters with high sequence conservation that are maintained due to strong purifying selection and concerted evolution. Photoprotein-like genes were also identified in the genomes of the non-luminescent sponge Amphimedon queenslandica and the non-luminescent cnidarian Nematostella vectensis, and phylogenomic analysis demonstrated that photoprotein genes arose at the base of all animals. Photoprotein gene expression in Mnemiopsis embryos begins during gastrulation in migrating precursors to photocytes and persists throughout development in the canals where photocytes reside. We identified three putative opsin genes in the Mnemiopsis genome and show that they do not group with well-known bilaterian opsin subfamilies. Interestingly, photoprotein transcripts are co-expressed with two of the putative opsins in developing photocytes. Opsin expression is also seen in the apical sensory organ. We present evidence that one opsin functions as a photopigment in vitro, absorbing light at wavelengths that overlap with peak photoprotein light emission, raising the hypothesis that light production and light reception may be functionally connected in ctenophore photocytes. We also present genomic evidence of a complete ciliary phototransduction cascade in Mnemiopsis.

Conclusions

This study elucidates the genomic organization, evolutionary history, and developmental expression of photoprotein and opsin genes in the ctenophore Mnemiopsis leidyi, introduces a novel dual role for ctenophore photocytes in both bioluminescence and phototransduction, and raises the possibility that light production and light reception are linked in this early-branching non-bilaterian animal.

Keywords:
Bioluminescence; ctenophore; Mnemiopsis leidyi; opsin; photocyte; photoprotein; photoreception; phototransduction