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

• Type of Material: Article
• Authors: Christine E. Schnitzler, National Institutes of Health; Kevin Pang, Sars International Centre for Marine Molecular Biology; Meghan L. Powers, Monterey Bay Aquarium Research Institute; Adam M. Reitzel, University of North Carolina; Joseph F. Ryan, Sars International Centre for Marine Molecular Biology; David Simmons, University of Hawaii; Takashi Tada, Emory University; Morgan Park, National Institutes of Health; Jyoti Gupta, National Institutes of Health; Shelise Y. Brooks, National Institutes of Health; Robert W. Blakesley, National Institutes of Health; Shozo Yokoyama, Emory University; Steven H.D. Haddock, Monterey Bay Aquarium Research Institute; Mark Q. Martindale, University of Hawaii; Andreas D. Baxevanis, National Institutes of Health
• Language: English
• Date: 2012-12-21
• Publisher: BioMed Central
• Publication Version: Final Published Version
• Copyright Statement: © 2012 Schnitzler et al; licensee BioMed Central Ltd.
• License: Creative Commons Attribution 2.0 Generic
• Final Published Version (URL): http://www.biomedcentral.com/1741-7007/10/107
• Title of Journal or Parent Work: BMC Biology
• ISSN: 1741-7007
• Volume: 10
• Issue: 107
• Start Page: 1
• End Page: 26
• Grant/Funding Information: MP and SHDH were supported by Award Number GM087198, National Institute of General Medical Sciences, NIH.; SY was supported by Award Number EY016400, National Eye Institute, NIH.; In addition, AMR was supported by Award Number F32HD062178 from the Eunice Kennedy Shriver National Institute of Child Health & Human Development, NIH.; This research was supported by the Intramural Research Program of the National Human Genome Research Institute, National Institutes of Health (NIH).
• Keywords: photocyte; Bioluminescence; photoreception; opsin; Mnemiopsis leidyi; phototransduction; photoprotein; ctenophore
• Research Categories: Biology, Genetics; Biology, Molecular

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.