Animals sense light primarily by an opsin-based photopigment present in a photoreceptor cell. Cnidaria are arguably the most basal phylum containing a well-developed visual system. The evolutionary history of opsins in the animal kingdom has not yet been resolved. Here, we study the evolution of animal opsins by genome-wide analysis of the cubozoan jellyfish Tripedalia cystophora, a cnidarian possessing complex lens-containing eyes and minor photoreceptors. A large number of opsin genes with distinct tissue- and stage-specific expression were identified. Our phylogenetic analysis unequivocally classifies cubozoan opsins as a sister group to c-opsins and documents lineage-specific expansion of the opsin gene repertoire in the cubozoan genome. Functional analyses provided evidence for the use of the Gs-cAMP signaling pathway in a small set of cubozoan opsins, indicating the possibility that the majority of other cubozoan opsins signal via distinct pathways. Additionally, these tests uncovered subtle differences among individual opsins, suggesting possible fine-tuning for specific photoreceptor tasks. Based on phylogenetic, expression and biochemical analysis we propose that rapid lineage- and species-specific duplications of the intron-less opsin genes and their subsequent functional diversification promoted evolution of a large repertoire of both visual and extraocular photoreceptors in cubozoans.

Department of Cell Differentiation Institute of Molecular Genetics Videnska 1083 Prague CZ 14220 Czech Republic

Department of Genomics and Bioinformatics Institute of Molecular Genetics Videnska 1083 Prague CZ 14220 Czech Republic

Department of Transcriptional Regulation Institute of Molecular Genetics Videnska 1083 Prague CZ 14220 Czech Republic

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Sci Rep. 2015 Sep 24;5:14396. doi: 10.1038/srep14396. PubMed

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Terakita A. The opsins. Genome Biol 6, 213, 10.1186/gb-2005-6-3-213 (2005). PubMed DOI PMC

Sakmar T. P., Menon S. T., Marin E. P. & Awad E. S. Rhodopsin: insights from recent structural studies. Annual Review of Biophysics and Biomolecular Structure 31, 443- 484, 10.1146/annurev.biophys.31.082901.134348 (2002). PubMed DOI

Porter M. L. et al. Shedding new light on opsin evolution. Proc Biol Sci 279, 3–14, 10.1098/rspb.2011.1819 (2012). PubMed DOI PMC

Suga H., Schmid V. & Gehring W. J. Evolution and functional diversity of jellyfish opsins. Current Biology 18, 51–55, 10.1016/j.cub.2007.11.059 (2008). PubMed DOI

Plachetzki D. C., Degnan B. M. & Oakley T. H. The origins of novel protein interactions during animal opsin evolution. PLoS One 2, e1054, 10.1371/journal.pone.0001054 (2007). PubMed DOI PMC

Feuda R., Hamilton S. C., McInerney J. O. & Pisani D. Metazoan opsin evolution reveals a simple route to animal vision. Proceedings of the National Academy of Sciences of the United States of America 109, 18868–18872, 10.1073/pnas.1204609109 (2012). PubMed DOI PMC

Kojima D. et al. A novel Go-mediated phototransduction cascade in scallop visual cells. Journal of Biological Chemistry 272, 22979–22982 (1997). PubMed

Koyanagi M., Terakita A., Kubokawa K. & Shichida Y. Amphioxus homologs of Go-coupled rhodopsin and peropsin having 11-cis- and all-trans-retinals as their chromophores. FEBS Letters 531, 525–528 (2002). PubMed

Hara T. & Hara R. Rhodopsin and retinochrome in the squid retina. Nature 214, 573–575 (1967). PubMed

Plachetzki D. C., Fong C. R. & Oakley T. H. The evolution of phototransduction from an ancestral cyclic nucleotide gated pathway. Proc Biol Sci 277, 1963–1969, 10.1098/rspb.2009.1797 (2010). PubMed DOI PMC

Feuda R., R.-S. O., Oakley T. H. & Pisani D. The comb jelly opsins and the origins of animal phototransduction. Genome Biology and Evolution 6, 1964-1971, 10.1093/gbe/evu154 (2014). PubMed DOI PMC

Marin E. P. et al. The amino terminus of the fourth cytoplasmic loop of rhodopsin modulates rhodopsin-transducin interaction. Journal of Biological Chemistry 275, 1930–1936 (2000). PubMed

Martin V. J. Photoreceptors of cnidarians. Can. J. Zool. 80, 1703–1722, 10.1139/Z02-136 (2002). DOI

Nilsson D. E., Gislen L., Coates M. M., Skogh C. & Garm A. Advanced optics in a jellyfish eye. Nature 435, 201–205, 10.1038/nature03484 (2005). PubMed DOI

Coates M. M. Visual ecology and functional morphology of cubozoa (cnidaria). Integr Comp Biol 43, 542–548, 10.1093/icb/43.4.542 (2003). PubMed DOI

O’Connor M., Nilsson D. E. & Garm A. Temporal properties of the lens eyes of the box jellyfish Tripedalia cystophora. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 196, 213–220, 10.1007/s00359-010-0506-8 (2010). PubMed DOI PMC

Garm A., Oskarsson M. & Nilsson D. E. Box jellyfish use terrestrial visual cues for navigation. Current Biology 21, 798–803, 10.1016/j.cub.2011.03.054 (2011). PubMed DOI

Petie R., Garm A. & Nilsson D. E. Visual control of steering in the box jellyfish Tripedalia cystophora. Journal of Experimental Biology 214, 2809–2815, 10.1242/jeb.057190 (2011). PubMed DOI

Land M. F. & Nilsson D. E. Animal eyes. Oxford, Oxford University Press (2002).

Kozmik Z. et al. Role of Pax genes in eye evolution: a cnidarian PaxB gene uniting Pax2 and Pax6 functions. Dev Cell 5, 773–785 (2003). PubMed

Piatigorsky J. & Kozmik Z. Cubozoan jellyfish: an Evo/Devo model for eyes and other sensory systems. International Journal of Developmental Biology 48, 719–-729., 10.1387/ijdb.041851jp (2004). PubMed DOI

Kozmik Z. et al. Assembly of the cnidarian camera-type eye from vertebrate-like components. Proceedings of the National Academy of Sciences of the United States of America 105, 8989–8993, 10.1073/pnas.0800388105 (2008). PubMed DOI PMC

Kozmik Z. et al. Cubozoan crystallins: evidence for convergent evolution of pax regulatory sequences. Evol Dev 10, 52–61, 10.1111/j.1525-142X.2007.00213.x (2008). PubMed DOI

O’Connor M., Garm A. & Nilsson D. E. Structure and optics of the eyes of the box jellyfish Chiropsella bronzie. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 195, 557–569, 10.1007/s00359-009-0431-x (2009). PubMed DOI

Parkefelt L., Skogh C., Nilsson D. E. & Ekstrom P. Bilateral symmetric organization of neural elements in the visual system of a coelenterate, Tripedalia cystophora (Cubozoa). Journal of Comparative Neurology 492, 251–262, 10.1002/cne.20658 (2005). PubMed DOI

Garm A., Andersson F. & Nilsson D. E. Unique structure and optics of the lesser eyes of the box jellyfish Tripedalia cystophora. Vision Research 48, 1061–1073, 10.1016/j.visres.2008.01.019 (2008). PubMed DOI

Koyanagi M. et al. Jellyfish vision starts with cAMP signaling mediated by opsin-G(s) cascade. Proceedings of the National Academy of Sciences of the United States of America 105, 15576–15580, 10.1073/pnas.0806215105 (2008). PubMed DOI PMC

Panda S. et al. Illumination of the melanopsin signaling pathway. Science 307, 600–604, 10.1126/science.1105121 (2005). PubMed DOI

Yamashita T. et al. Opn5 is a UV-sensitive bistable pigment that couples with Gi subtype of G protein. Proceedings of the National Academy of Sciences of the United States of America 107, 22084–22089, 10.1073/pnas.1012498107 (2010). PubMed DOI PMC

Bridge D., Cunningham C. W., Schierwater B., DeSalle R. & Buss L. W. Class-level relationships in the phylum Cnidaria: evidence from mitochondrial genome structure. Proceedings of the National Academy of Sciences of the United States of America 89, 8750–8753 (1992). PubMed PMC

Bailes H. J., Lucas, Z. L. R. J. Reproducible and sustained regulation of Gαs signalling using a metazoan opsin as an optogenetic tool. PLOS one 7, 10.1371/journal.pone.0030774 (2012). PubMed DOI PMC

Koyanagi M., Kubokawa K., Tsukamoto H., Shichida Y. & Terakita A. Cephalochordate melanopsin: evolutionary linkage between invertebrate visual cells and vertebrate photosensitive retinal ganglion cells. Current Biology 15, 1065–1069, 10.1016/j.cub.2005.04.063 (2005). PubMed DOI

Hohenegger M. et al. Gsalpha-selective G protein antagonists. Proceedings of the National Academy of Sciences of the United States of America 95, 346–351 (1998). PubMed PMC

Shabalina S. A. et al. Distinct patterns of expression and evolution of intronless and intron-containing mammalian genes. Molecular biology and evolution 27, 1745–1749, 10.1093/molbev/msq086 (2010). PubMed DOI PMC

Zou M., Guo B. & He S. The roles and evolutionary patterns of intronless genes in deuterostomes. Comparative and functional genomics 2011, 680673, 10.1155/2011/680673 (2011). PubMed DOI PMC

Gentles A. J. & Karlin S. Why are human G-protein-coupled receptors predominantly intronless? Trends in genetics : TIG 15, 47–49 (1999). PubMed

Brosius J. Many G-protein-coupled receptors are encoded by retrogenes. Trends in genetics : TIG 15, 304–305 (1999). PubMed

Fridmanis D., Fredriksson R., Kapa I., Schioth H. B. & Klovins J. Formation of new genes explains lower intron density in mammalian Rhodopsin G protein-coupled receptors. Molecular phylogenetics and evolution 43, 864–880, 10.1016/j.ympev.2006.11.007 (2007). PubMed DOI

UCSC, G. B. G. Opsin evolution: update blog http://genomewiki.ucsc.edu, (Date of acces: 20/05/2012).

Morris A. B. J. & Hunt D. M. The molecular basis of a spectral shift in the rhodopsin of two species of squid from different photic enviroments. Proceedings of the Royal Society of London B 254, 233–240 (1993). PubMed

Fitzgibbon J., , Slobodvanyuk S. J., Bellingham J., Bowmaker J. K. & Hunt D. M. The rhodopsin-encoding gene of bony fish lacks introns. Gene 164, 273–277 (1995). PubMed

Innan H. & Kondrashov F. The evolution of gene duplications: classifying and distinguishing between models. Nature reviews. Genetics 11, 97–108, 10.1038/nrg2689 (2010). PubMed DOI

Lynch M. & Conery J. S. The evolutionary fate and consequences of duplicate genes. Science (New York, N.Y.) 290, 1151–1155 (2000). PubMed

Matsumoto Y., Fukamachi S., Mitani H. & Kawamura S. Functional characterization of visual opsin repertoire in Medaka (Oryzias latipes). Gene 371, 268–278, 10.1016/j.gene.2005.12.005 (2006). PubMed DOI

Rennison D. J., Owens G. L. & Taylor J. S. Opsin gene duplication and divergence in ray-finned fish. Molecular phylogenetics and evolution 62, 986–1008, 10.1016/j.ympev.2011.11.030 (2012). PubMed DOI

Skogh C., Garm A., Nilsson D. E. & Ekstrom P. Bilaterally symmetrical rhopalial nervous system of the box jellyfish Tripedalia cystophora. Journal of Morphology 267, 1391–1405, 10.1002/jmor.10472 (2006). PubMed DOI

Garm A., Ekstrom P., Boudes M. & Nilsson D. E. Rhopalia are integrated parts of the central nervous system in box jellyfish. Cell Tissue Res 325, 333–343, 10.1007/s00441-005-0134-8 (2006). PubMed DOI

Stockl A. L., Petie R. & Nilsson D. E. Setting the pace: new insights into central pattern generator interactions in box jellyfish swimming. PLoS One 6, e27201, 10.1371/journal.pone.0027201 (2011). PubMed DOI PMC

Yamasu T. & Yoshida M. Fine structure of complex ocelli of a cubomedusan, Tamoya bursaria Haeckel. Cell and Tissue Research 170, 325–339 (1976). PubMed

Laska G., Hundgen, M. Morphologie und ultrastruktur der lichtsinnesorgane von Tripedalia cystophora Conant (Cnidaria, Cubozoa). Zool Jb Anat 108, 107–123 (1982).

O’Connor M. et al. Visual pigment in the lens eyes of the box jellyfish Chiropsella bronzie. Proc Biol Sci 277, 1843–1848, 10.1098/rspb.2009.2248 (2010). PubMed DOI PMC

Ekstrom P., Garm A., Palsson J., Vihtelic T. S. & Nilsson D. E. Immunohistochemical evidence for multiple photosystems in box jellyfish. Cell and Tissue Research 333, 115–124, 10.1007/s00441-008-0614-8 (2008). PubMed DOI

Garm A. & Ekstrom P. Evidence for multiple photosystems in jellyfish. Int Rev Cell Mol Biol 280, 41–78, 10.1016/s1937-6448(10)80002-4 (2010). PubMed DOI

Yoshida M. Extraocular photoreception. Handbook of sensory physiology VII/6A, 582–640 (1979).

Taddei-Ferretti C. & Musio C. Photobehaviour of Hydra (Cnidaria, Hydrozoa) and correlated mechanisms: a case of extraocular photosensitivity. Journal of Photochemistry and Photobiology. B, Biology 55, 88–101 (2000). PubMed

Arkett S. A. & Spencer A. N. Neuronal mechanism of a hydromedusan shadow reflex. I. Identified reflex components and sequence of events J. Comp. Physiol. A 159, 201–213 (1986).

Sawyer, S. J., D. H. B. & Shick M. Neurophysiological correlates of the behavioral response to light in the sea anemone Anthopleura elegantissima. Biol. Bull. (Woods Hole, Mass.) 186, 195–201 (1994). PubMed

Musio C. et al. First identification and localization of a visual pigment in Hydra (Cnidaria, Hydrozoa). J Comp Physiol A 187, 79–81 (2001). PubMed

Plachetzki D. C., Fong C. R. & Oakley T. H. Cnidocyte discharge is regulated by light and opsin-mediated phototransduction. BMC Biol 10, 17, 10.1186/1741-7007-10-17 (2012). PubMed DOI PMC

Mason B. et al. Evidence for multiple phototransduction pathways in a reef-building coral. PLoS One 7, e50371, 10.1371/journal.pone.0050371 (2012). PubMed DOI PMC

Nordstrom K., Wallen R., Seymour J. & Nilsson D. A simple visual system without neurons in jellyfish larvae. Proc Biol Sci 270, 2349–2354, 10.1098/rspb.2003.2504 (2003). PubMed DOI PMC

Koyanagi M.T. E., Nagata T., Tsukamoto H. & Terakita A. Homologs of vertebrate Opn3 potentially serve as a light sensor in nonphotoreceptive tissue. Proceeding of the National Academy of Sciences of the United States of America 110, 4998–5003, 10.1073/pnas.1219416110 (2013). PubMed DOI PMC

Heck M. S. S., Maretzki D., Bartl F. J., Ritter E., Palczewski K.& Hofmann K. P. Signaling States of Rhodopsin: FORMATION OF THE STORAGE FORM, METARHODOPSIN III, FROM ACTIVE METARHODOPSIN II. Journal of Biological Chemistry 278, 3162–3169 (2003). PubMed PMC

Pearson W. R. & Lipman D. J. Improved tools for biological sequence comparison. Proceedings of the National Academy of Sciences of the United States of America 85, 2444–2448 (1988). PubMed PMC

Guindon S. et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59, 307–321, 10.1093/sysbio/syq010 (2010). PubMed DOI

Le S. Q. & Gascuel O. An improved general amino acid replacement matrix. Molecular Biology and Evolution 25, 1307–1320, 10.1093/molbev/msn067 (2008). PubMed DOI

Anisimova M. & Gascuel O. Approximate likelihood-ratio test for branches: A fast, accurate, and powerful alternative. Syst Biol 55, 539–552, 10.1080/10635150600755453 (2006). PubMed DOI

Larkin M. A. et al. Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947–2948, 10.1093/bioinformatics/btm404 (2007). PubMed DOI

The role of transposable elements in functional evolution of amphioxus genome: the case of opsin gene family