Abstract Opsin proteins are central to photoreception and have diversified extensively to support both visual and non-visual functions in animals. While the molecular conservation is striking, the evolutionary pathways that shaped opsin diversity, particularly in relation to visual and extraocular roles, remain poorly understood. To address this gap, we examined opsin expression in Pteriomorphia, a diverse group of mostly sessile marine bivalves with multiple photoreceptor systems and ecologies. We generated transcriptomes for 12 species, including eyed and eyeless adults, and analysed published RNA-seq data from five additional species covering all taxonomic orders and eye types. We identified and classified opsins expressed in the photosensitive mantle margin and eyes using phylogenetically informed annotation. We tested whether opsin diversity is associated with eye presence or mobility and determined which opsins are widely used. Our results suggest that bivalve eyes generally express more opsins than extraocular tissues. Additionally, convergent expansions and reductions of opsin diversity were estimated, likely derived from an ancestral repertoire in the mantle margin. Curiously, differences in mobility among species do not influence opsin repertoire. Our findings further support that the rhodopsin-retinochrome system is pervasive across bivalves and identify visual and non-visual opsins used in both eyes and dermal photoreception.
more »
« less
Opsin expression varies across larval development and taxa in pteriomorphian bivalves
Many marine organisms have a biphasic life cycle that transitions between a swimming larva with a more sedentary adult form. At the end of the first phase, larvae must identify suitable sites to settle and undergo a dramatic morphological change. Environmental factors, including photic and chemical cues, appear to influence settlement, but the sensory receptors involved are largely unknown. We targeted the protein receptor, opsin, which belongs to large superfamily of transmembrane receptors that detects environmental stimuli, hormones, and neurotransmitters. While opsins are well-known for light-sensing, including vision, a growing number of studies have demonstrated light-independent functions. We therefore examined opsin expression in the Pteriomorphia, a large, diverse clade of marine bivalves, that includes commercially important species, such as oysters, mussels, and scallops. Methods Genomic annotations combined with phylogenetic analysis show great variation of opsin abundance among pteriomorphian bivalves, including surprisingly high genomic abundance in many species that are eyeless as adults, such as mussels. Therefore, we investigated the diversity of opsin expression from the perspective of larval development. We collected opsin gene expression in four families of Pteriomorphia, across three distinct larval stages, i.e., trochophore, veliger, and pediveliger, and compared those to adult tissues.Results We found larvae express all opsin types in these bivalves, but opsin expression patterns are largely species-specific across development. Few opsins are expressed in the adult mantle, but many are highly expressed in adult eyes. Intriguingly, opsin genes such as retinochrome, xenopsins, and Go-opsins have higher levels of expression in the later larval stages when substrates for settlement are being tested, such as the pediveliger. Conclusion Investigating opsin gene expression during larval development provides crucial insights into their intricate interactions with the surroundings, which may shed light on how opsin receptors of these organisms respond to various environmental cues that play a pivotal role in their settlement process.
more »
« less
- Award ID(s):
- 2148203
- PAR ID:
- 10530600
- Publisher / Repository:
- Frontiersin.org
- Date Published:
- Journal Name:
- Frontiers in Neuroscience
- Volume:
- 18
- ISSN:
- 1662-453X
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Synopsis Opsins are G-protein-coupled receptors often expressed in neuronal photoreceptor cells and used for light detection in most animals, including cnidarians like corals, jellyfish, and anemones. Opsins may also be expressed in non-neuronal cell types, where they may confer light sensitivity. For example, opsins might be involved in pre-neural phototaxis of larval box jellyfish. However, the overall extent of non-neuronal expression of opsins is not well understood, despite the potential for identifying additional light or opsin-mediated organismal functions. To investigate the prevalence of non-neuronal opsin expression in a cnidarian, we analyzed published data from Hydra vulgaris, a freshwater hydroid that responds to light despite lacking distinct photosensory structures such as eyes. We quantified opsin expression across Hydra cell types and states of cell differentiation using published single-cell RNA sequencing (scRNA-seq) data and assay for transposase-accessible chromatin sequencing data. We identified 45 opsin transcripts in Hydra expressed in neuronal and non-neuronal cell types, as well as across inferred states of cell differentiation. We found a wider diversity of opsin gene transcripts in neuronal cell types, predominantly in fully differentiated cells. In contrast, we detected fewer opsin transcripts in non-neuronal cell types, and they were expressed from stem cell to progenitor cell to fully differentiated cell state—all within the same inferred cell type. These opsin transcripts appear to be expressed at higher levels in ectodermal epithelial cells near the head organizer of Hydra (a key developmental patterning region) and share transcription factor binding motifs with development genes such as Six, Otx, Ptx, Rfx4, and Hxa. Overall, we outline an array of opsin gene transcripts, their expression, and open chromatin patterns across cell type diversity in Hydra, and highlight potential co-regulatory relationships that may pave the way for future work on unconventional roles for opsin genes in Hydra.more » « less
-
Rokas, A (Ed.)Abstract The bivalve subclass Pteriomorphia, which includes the economically important scallops, oysters, mussels, and ark clams, exhibits extreme ecological, morphological, and behavioral diversity. Among this diversity are five morphologically distinct eye types, making Pteriomorphia an excellent setting to explore the molecular basis for the evolution of novel traits. Of pteriomorphian bivalves, Limida is the only order lacking genomic resources, greatly limiting the potential phylogenomic analyses related to eyes and phototransduction. Here, we present a limid genome assembly, the disco clam, Ctenoides ales (C. ales), which is characterized by invaginated eyes, exceptionally long tentacles, and a flashing light display. This genome assembly was constructed with PacBio long reads and Dovetail Omni-CTM proximity-ligation sequencing. The final assembly is ∼2.3Gb and over 99% of the total length is contained in 18 pseudomolecule scaffolds. We annotated 41,064 protein coding genes and reported a BUSCO completeness of 91.9% for metazoa_obd10. Additionally, we report a complete and annotated mitochondrial genome, which also had been lacking from Limida. The ∼20Kb mitogenome has 12 protein coding genes, 22 tRNAs, 2 rRNA genes, and a 1,589 bp duplicated sequence containing the origin of replication. The C. ales nuclear genome size is substantially larger than other pteriomorphian genomes, mainly accounted for by transposable element sequences. We inventoried the genome for opsins, the signaling proteins that initiate phototransduction, and found that, unlike its closest eyed-relatives, the scallops, C. ales lacks duplication of the rhabdomeric Gq-protein-coupled opsin that is typically used for invertebrate vision. In fact, C. ales has uncharacteristically few opsins relative to the other pteriomorphian families, all of which have unique expansions of xenopsins, a recently discovered opsin subfamily. This chromosome-level assembly, along with the mitogenome, is a valuable resource for comparative genomics and phylogenetics in bivalves and particularly for the understudied but charismatic limids.more » « less
-
Battistuzzi, Fabia Ursula (Ed.)Abstract In animals, opsins and cryptochromes are major protein families that transduce light signals when bound to light-absorbing chromophores. Opsins are involved in various light-dependent processes, like vision, and have been co-opted for light-independent sensory modalities. Cryptochromes are important photoreceptors in animals, generally regulating circadian rhythm, they belong to a larger protein family with photolyases, which repair UV-induced DNA damage. Mollusks are great animals to explore questions about light sensing as eyes have evolved multiple times across, and within, taxonomic classes. We used molluscan genome assemblies from 80 species to predict protein sequences and examine gene family evolution using phylogenetic approaches. We found extensive opsin family expansion and contraction, particularly in bivalve xenopsins and gastropod Go-opsins, while other opsins, like retinochrome, rarely duplicate. Bivalve and gastropod lineages exhibit fluctuations in opsin repertoire, with cephalopods having the fewest number of opsins and loss of at least 2 major opsin types. Interestingly, opsin expansions are not limited to eyed species, and the highest opsin content was seen in eyeless bivalves. The dynamic nature of opsin evolution is quite contrary to the general lack of diversification in mollusk cryptochromes, though some taxa, including cephalopods and terrestrial gastropods, have reduced repertoires of both protein families. We also found complete loss of opsins and cryptochromes in multiple, but not all, deep-sea species. These results help set the stage for connecting genomic changes, including opsin family expansion and contraction, with differences in environmental, and biological features across Mollusca.more » « less
-
Salmonids are ideal models as many species follow a distinct developmental program from demersal eggs and a large yolk sac to hatching at an advanced developmental stage. Further, these economically important teleosts inhabit both marine- and freshwaters and experience diverse light environments during their life histories. At a genome level, salmonids have undergone a salmonid-specific fourth whole genome duplication event (Ss4R) compared to other teleosts that are already more genetically diverse compared to many non-teleost vertebrates. Thus, salmonids display phenotypically plastic visual systems that appear to be closely related to their anadromous migration patterns. This is most likely due to a complex interplay between their larger, more gene-rich genomes and broad spectrally enriched habitats; however, the molecular basis and functional consequences for such diversity is not fully understood. This study used advances in genome sequencing to identify the repertoire and genome organization of visual opsin genes (those primarily expressed in retinal photoreceptors) from six different salmonids [Atlantic salmon ( Salmo salar ), brown trout ( Salmo trutta ), Chinook salmon ( Oncorhynchus tshawytcha ), coho salmon ( Oncorhynchus kisutch ), rainbow trout ( Oncorhynchus mykiss ), and sockeye salmon ( Oncorhynchus nerka )] compared to the northern pike ( Esox lucius ), a closely related non-salmonid species. Results identified multiple orthologues for all five visual opsin classes, except for presence of a single short-wavelength-sensitive-2 opsin gene. Several visual opsin genes were not retained after the Ss4R duplication event, which is consistent with the concept of salmonid rediploidization. Developmentally, transcriptomic analyzes of Atlantic salmon revealed differential expression within each opsin class, with two of the long-wavelength-sensitive opsins not being expressed before first feeding. Also, early opsin expression in the retina was located centrally, expanding dorsally and ventrally as eye development progressed, with rod opsin being the dominant visual opsin post-hatching. Modeling by spectral tuning analysis and atomistic molecular simulation, predicted the greatest variation in the spectral peak of absorbance to be within the Rh2 class, with a ∼40 nm difference in λ max values between the four medium-wavelength-sensitive photopigments. Overall, it appears that opsin duplication and expression, and their respective spectral tuning profiles, evolved to maximize specialist color vision throughout an anadromous lifecycle, with some visual opsin genes being lost to tailor marine-based vision.more » « less
An official website of the United States government

