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

Abstract

BackgroundCalcium-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.ResultsThe 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.ConclusionsThis 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.

Novel Structures Associated with Presumed Photoreceptors in the Aboral Sense Organ of Ctenophores

“…Second, it is remarkable that the geometrical arrangement of the four bristle groups corresponds so closely to that of the four groups of lamellate bodies, which ultrastructural (1) and molecular-genomic evidence (17) indicate are photoreceptors. Not believing in anatomical coincidences leads one to believe that the bristle groups may somehow be involved in photoreception by ctenophores.…”

Elements of a ‘nervous system’ in sponges

“…The absence of any opsins in sponges is curious because opsins are known from plants and fungi (microbial, type I opsins) and are thought to be convergent with animal type II opsins (Heintzen, 2012). At least two rhabdomeric (type II) opsins have been found in ctenophores (Schnitzler et al, 2012). Were opsins, like nerves, also lost in sponges?…”

“…If one compares just the sensory systems of sponges and ctenophores, it hardly seems likely that sponges have lost nerves. Sensory organs in ctenophores are sophisticated -both the balancer organ of the cydippid larva and of the adult in Pleurobrachia (Tamm and Tamm, 2002) and the photosensory molecules, including opsins of Mnemiopsis (Schnitzler et al, 2012) reflect a complexity not seen in any sponge. Ctenophore nerves use glutamate in signalling, while GABA appears in muscle (Ryan et al, 2013;Moroz et al, 2014).…”

Convergent evolution of neural systems in ctenophores

“…The activity of cilia is under control of the aboral organ composed of several cell types with gravity sensors and a statolith consisting of about 100 lithocytes (Tamm, 1973;Tamm, 1982). In addition, there is a diversity of mechano-and chemoreceptors (Aronova and Alekseeva, 2003; Kass-Simon and Hufnagel, 1992) as well as putative photosensors; but no morphologically defined eyes or photoreceptors were described (Anctil and Shimomura, 1984;Girsch and Hastings, 1978;Horridge, 1964b;Schnitzler et al, 2012;Vinnikov, 1990). The structural relationships and functional interactions among different neural elements are mostly unknown.…”