title: Genomic organization, evolution, and expression of photoprotein and opsin genes in Mnemiopsis leidyi: a new view of ctenophore photocytes.
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.
authors.affiliation: National Human Genome Research Institute, National Institutes of Health, Bethesda, MD 20892, USA.
authors.forename: Christine E
authors.initials: CE
authors.lastname: Schnitzler
authors.forename: Kevin
authors.initials: K
authors.lastname: Pang
authors.forename: Meghan L
authors.initials: ML
authors.lastname: Powers
authors.forename: Adam M
authors.initials: AM
authors.lastname: Reitzel
authors.forename: Joseph F
authors.initials: JF
authors.lastname: Ryan
authors.forename: David
authors.initials: D
authors.lastname: Simmons
authors.forename: Takashi
authors.initials: T
authors.lastname: Tada
authors.forename: Morgan
authors.initials: M
authors.lastname: Park
authors.forename: Jyoti
authors.initials: J
authors.lastname: Gupta
authors.forename: Shelise Y
authors.initials: SY
authors.lastname: Brooks
authors.forename: Robert W
authors.initials: RW
authors.lastname: Blakesley
authors.forename: Shozo
authors.initials: S
authors.lastname: Yokoyama
authors.forename: Steven Hd
authors.initials: SH
authors.lastname: Haddock
authors.forename: Mark Q
authors.initials: MQ
authors.lastname: Martindale
authors.forename: Andreas D
authors.initials: AD
authors.lastname: Baxevanis
mesh_terms: D000595:Amino Acid Sequence; D000818:Animals; D016000:Cluster Analysis; D037302:Ctenophora / Q000166:cytology* / Q000235:genetics* / Q000528:radiation effects; D019143:Evolution, Molecular; D005786:Gene Expression Regulation / Q000528:radiation effects; D016678:Genome / Q000235:genetics*; D049452:Green Fluorescent Proteins / Q000378:metabolism; D008027:Light; D055537:Light Signal Transduction / Q000528:radiation effects; D008164:Luminescent Proteins / Q000737:chemistry / Q000235:genetics* / Q000378:metabolism; D008969:Molecular Sequence Data; D055355:Opsins / Q000737:chemistry / Q000235:genetics* / Q000378:metabolism; D010802:Phylogeny; D012333:RNA, Messenger / Q000235:genetics / Q000378:metabolism; D015203:Reproducibility of Results; D012641:Selection, Genetic; D016415:Sequence Alignment; D020539:Sequence Analysis, Protein; D013057:Spectrum Analysis
chemical_list: D008164:Luminescent Proteins; D055355:Opsins; D012333:RNA, Messenger; D049452:Green Fluorescent Proteins