Nematostella vectensis exemplifies the exceptional expansion and diversity of opsins in the eyeless Hexacorallia
Abstract 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...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2023-09-01
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| Series: | EvoDevo |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s13227-023-00218-8 |
| _version_ | 1797452352451510272 |
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| author | Kyle J. McCulloch Leslie S. Babonis Alicia Liu Christina M. Daly Mark Q. Martindale Kristen M. Koenig |
| author_facet | Kyle J. McCulloch Leslie S. Babonis Alicia Liu Christina M. Daly Mark Q. Martindale Kristen M. Koenig |
| author_sort | Kyle J. McCulloch |
| collection | DOAJ |
| description | Abstract 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 anemone Nematostella 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 from N. 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 of NvOpsins and 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 in N. vectensis suggest 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. |
| first_indexed | 2024-03-09T15:07:35Z |
| format | Article |
| id | doaj.art-1ca6c459d36140a0a33943ce8c674aab |
| institution | Directory Open Access Journal |
| issn | 2041-9139 |
| language | English |
| last_indexed | 2024-03-09T15:07:35Z |
| publishDate | 2023-09-01 |
| publisher | BMC |
| record_format | Article |
| series | EvoDevo |
| spelling | doaj.art-1ca6c459d36140a0a33943ce8c674aab2023-11-26T13:34:35ZengBMCEvoDevo2041-91392023-09-0114111910.1186/s13227-023-00218-8Nematostella vectensis exemplifies the exceptional expansion and diversity of opsins in the eyeless HexacoralliaKyle J. McCulloch0Leslie S. Babonis1Alicia Liu2Christina M. Daly3Mark Q. Martindale4Kristen M. Koenig5Department of Ecology, Evolution and Behavior, University of MinnesotaDepartment of Ecology and Evolutionary Biology, Cornell UniversityJohn Harvard Distinguished Science Fellowship Program, Harvard UniversityJohn Harvard Distinguished Science Fellowship Program, Harvard UniversityWhitney Lab for Marine Bioscience, University of FloridaJohn Harvard Distinguished Science Fellowship Program, Harvard UniversityAbstract 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 anemone Nematostella 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 from N. 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 of NvOpsins and 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 in N. vectensis suggest 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.https://doi.org/10.1186/s13227-023-00218-8NematostellaSea anemoneOpsinRhodopsinPhotoreceptorCnidaria |
| spellingShingle | Kyle J. McCulloch Leslie S. Babonis Alicia Liu Christina M. Daly Mark Q. Martindale Kristen M. Koenig Nematostella vectensis exemplifies the exceptional expansion and diversity of opsins in the eyeless Hexacorallia EvoDevo Nematostella Sea anemone Opsin Rhodopsin Photoreceptor Cnidaria |
| title | Nematostella vectensis exemplifies the exceptional expansion and diversity of opsins in the eyeless Hexacorallia |
| title_full | Nematostella vectensis exemplifies the exceptional expansion and diversity of opsins in the eyeless Hexacorallia |
| title_fullStr | Nematostella vectensis exemplifies the exceptional expansion and diversity of opsins in the eyeless Hexacorallia |
| title_full_unstemmed | Nematostella vectensis exemplifies the exceptional expansion and diversity of opsins in the eyeless Hexacorallia |
| title_short | Nematostella vectensis exemplifies the exceptional expansion and diversity of opsins in the eyeless Hexacorallia |
| title_sort | nematostella vectensis exemplifies the exceptional expansion and diversity of opsins in the eyeless hexacorallia |
| topic | Nematostella Sea anemone Opsin Rhodopsin Photoreceptor Cnidaria |
| url | https://doi.org/10.1186/s13227-023-00218-8 |
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