Light modulated cnidocyte discharge predates the origins of eyes in Cnidaria

Picciani, Natasha; Kerlin, Jamie R.; Jindrich, Katia; Hensley, Nicholai M.; Gold, David A.; Oakley, Todd H.

doi:10.1002/ece3.7280

Cited by 10 publications

(4 citation statements)

References 46 publications

(57 reference statements)

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“…The neurite-like structures stained in the tentacles are perhaps involved in modulating cnidocyte discharge based on the light level. In a diversity of polyp stages across cnidarian taxa, the discharge of the nematocytes on the tentacles is influenced by the ambient light (Plachetzki et al, 2012;Picciani et al, 2021). We expect this function to be present in most cnidarians including box jellyfish, which display a strict diurnal rhythm (Garm et al, 2012), and the staining patterns on the tentacles in between the nematocytes are exactly how we would expect the putative opsin-carrying neurons to be arranged.…”

Section: Extraocular Photoreceptorsmentioning

confidence: 86%

Expression of Opsins of the Box Jellyfish Tripedalia cystophora Reveals the First Photopigment in Cnidarian Ocelli and Supports the Presence of Photoisomerases

Garm

Svaerke²,

Pontieri³

et al. 2022

Front. Neuroanat.

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Cubomedusae, or box jellyfish, have a complex visual system comprising 24 eyes of four types. Like other cnidarians, their photoreceptor cells are ciliary in morphology, and a range of different techniques together show that at least two of the eye types—the image-forming upper and lower lens eyes—express opsin as the photopigment. The photoreceptors of these two eye types express the same opsin (Tc LEO), which belongs to the cnidarian-specific clade cnidops. Interestingly, molecular work has found a high number of opsin genes in box jellyfish, especially in the Caribbean species Tripedalia cystophora, most of which are of unknown function. In the current study, we raised antibodies against three out of five opsins identified from transcriptomic data from T. cystophora and used them to map the expression patterns. These expression patterns suggest one opsin as the photopigment in the slit eyes and another as a putative photoisomerase found in photoreceptors of all four eyes types. The last antibody stained nerve-like cells in the tentacles, in connection with nematocytes, and the radial nerve, in connection with the gonads. This is the first time photopigment expression has been localized to the outer segments of the photoreceptors in a cnidarian ocellus (simple eye). The potential presence of a photoisomerase could be another interesting convergence between box jellyfish and vertebrate photoreceptors, but it awaits final experimental proof.

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Section: Extraocular Photoreceptorsmentioning

confidence: 86%

Expression of Opsins of the Box Jellyfish Tripedalia cystophora Reveals the First Photopigment in Cnidarian Ocelli and Supports the Presence of Photoisomerases

Garm

Svaerke²,

Pontieri³

et al. 2022

Front. Neuroanat.

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“…Together these data suggest at least 3 major opsin clades existed in the ancestor of both Bilateria and Cnidaria [1,4,6,15,32]. Evidence from both eyed and eyeless cnidarians shows that cnidarian opsins function as photoreceptors using canonical phototransduction cascades [3,31,[33][34][35][36][37][38][39][40][41][42][43][44][45][46]. Both sequence homology and physiological evidence suggest cnidarian opsin biochemistry and function is similar to bilaterian opsins [47].…”

Section: Introductionmentioning

confidence: 83%

Nematostella vectensisexemplifies the exceptional expansion and diversity of opsins in the eyeless Hexacorallia

McCulloch

Babonis

Liu

et al. 2023

Preprint

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Background: Opsins are the primary proteins responsible for light detection in animals. Cnidarians (jellyfish, sea anemones, corals) have diverse visual systems that have evolved in parallel with bilaterians (squid, flies, fish) for hundreds of millions of years. Medusozoans (e.g. jellyfish, hydroids) have evolved eyes multiple times, each time independently incorporating distinct opsin orthologs. Anthozoans (e.g. corals, sea anemones,) have diverse light-mediated behaviors and, despite being eyeless, exhibit more extensive opsin duplications than medusozoans. To better understand the evolution of photosensitivity in animals without eyes we increased anthozoan representation in the phylogeny of animal opsins and investigated the large but poorly characterized opsin family in the sea anemoneNematostella vectensis. Results: We analyzed genomic and transcriptomic data from 16 species of cnidarians to generate a large opsin phylogeny (708 sequences) with the largest sampling of anthozoan sequences to date. We identified 29 opsins fromN. vectensis(NvOpsins) with high confidence, using transcriptomic and genomic datasets. We found that lineage-specific opsin duplications are common across Cnidaria, with anthozoan lineages exhibiting among the highest numbers of opsins in animals. To establish putative photosensory function of NvOpsins, we identified canonically conserved protein domains and amino acid sequences essential for opsin function in other animal species. We show high sequence diversity among NvOpsins at sites important for photoreception and transduction, suggesting potentially diverse functions. We further examined the spatiotemporal expression ofNvOpsinsand found both dynamic expression of opsins during embryonic development and sexually dimorphic opsin expression in adults. Conclusions: These data show that lineage-specific duplication and divergence has led to expansive diversity of opsins in eyeless cnidarians, suggesting opsins from these animals may exhibit novel biochemical functions. The variable expression patterns of opsins inN. vectensissuggest opsin gene duplications allowed for a radiation of unique sensory cell types with tissue- and stage-specific functions. This diffuse network of distinct sensory cell types could be an adaptive solution for varied sensory tasks experienced in distinct life history stages in anthozoans.

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“…The last common Cnidarian ancestor, as well as ancestors of Medusozoans including Hydrozoa (which contains the clade of Hydra vulgaris), have no eye. Cnidocyte discharge predated eyes, perhaps facilitating the evolution of eyes in Cnidarians (Picciani et al, 2021). RdCVF is a module that may have been involved in cnidocyte regeneration and was recruited for photoreceptor metabolism during evolution (Swafford and Oakley, 2019).…”

Section: The Trophic Factor Rdcvfmentioning

confidence: 99%

The Emergence of the Metabolic Signaling of the Nucleoredoxin-like Genes during Evolution

Aït-Ali

Blond

Clérin

et al. 2022

Preprint

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The nucleoredoxin-like genes NXNL1 and NXNL2 were identified through the biological activity of rod-derived cone viability factors (RdCVF and RdCVF2), the alternatively spliced variants produced by intron retention, that mediate signaling between rod and cone photoreceptors by stimulating glucose uptake. These therapeutic genes for inherited retinal degenerations also produce by splicing thioredoxin-like proteins that reduce oxidized cysteines in photoreceptor proteins. The first NXNL genes date from the first animal phyla. Intron retention produces an active RdCVF protein in the tentacles of Hydra vulgaris, a species without eyes. A Scallop RdCVF protein is produced by ciliated photoreceptors of the retina and binds its receptor, BSG1. In the lamprey, a descendent of early vertebrates, RdCVF metabolic signaling between rod and cones is fully established. In the mouse, the production of BSG1 by photoreceptors is regulated by cell-specific splicing inhibition. RdCVF signaling predates photoreceptors and evolved through two alternative splicing events.

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Light modulated cnidocyte discharge predates the origins of eyes in Cnidaria

Abstract: This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Cited by 10 publications

References 46 publications

Expression of Opsins of the Box Jellyfish Tripedalia cystophora Reveals the First Photopigment in Cnidarian Ocelli and Supports the Presence of Photoisomerases

Expression of Opsins of the Box Jellyfish Tripedalia cystophora Reveals the First Photopigment in Cnidarian Ocelli and Supports the Presence of Photoisomerases

Nematostella vectensisexemplifies the exceptional expansion and diversity of opsins in the eyeless Hexacorallia

The Emergence of the Metabolic Signaling of the Nucleoredoxin-like Genes during Evolution

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