Cubozoan genome illuminates functional diversification of opsins and photoreceptor evolution

Abstract

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.

The opsin repertoire of the European lancelet: a window into light detection in a basal chordate

“…The large scale phylogenetic relations of opsins has been the object of many studies (Albalat, 2012;Liegertova et al, 2015;Porter et al, 2012;Ramirez et al, 2016). We wanted to classify the B. lanceolatum opsins and investigate their distribution over the major opsin groups.…”

“…Their tissue specificity thus can significantly vary. Recent analyses of opsin gene expression in Cnidaria or Arthropoda documented a wide range of tissues where opsins can be detected (Liegertova et al, 2015;Battelle et al, 2016). Our study examined the expression pattern of opsins across multiple developmental stages ( Fig.…”

“…Ramirez and colleagues have proposed that a repertoire of at least nine opsin paralogs was present in the bilaterian ancestor (Ramirez et al, 2016). In regard to the cnidarian opsins, there are conflicting results regarding their position in the phylogenetic tree (Feuda et al, 2012;Liegertova et al, 2015;Plachetzki et al, 2007;Porter et al, 2012;Suga et al, 2008). The function of most opsins consists of two steps: light absorption and G-protein activation in both visual and non-visual systems.…”

“…The function of most opsins consists of two steps: light absorption and G-protein activation in both visual and non-visual systems. Isomerization of the chromophore 11-cis-retinaldehyde to all-trans-retinaldehyde due to light absorption, changes the conformation of the opsin and triggers a signal transduction cascade, the type of which is dependent on the G-protein to which the opsin binds Branchiostoma lanceolatum opsins 765 (Koyanagi et al, 2008;Liegertova et al, 2015;Yarfitz and Hurley, 1994). The conserved lysine in the seventh helix is used to form a Schiff-base bond to the retinal chromophore (Bownds, 1967;Wang et al, 1980) and in its protonated form it is stabilized by a negatively charged amino acid, called a counterion, whose position varies among different opsin subfamilies (reviewed in Porter et al, 2012;Shichida and Matsuyama, 2009).…”

The opsin repertoire of the Antarctic krill Euphausia superba

“…The role of this large number of opsins involved in visual and non-visual photoreception is still largely unknown. However, we could speculate that adaptation to complex marine and freshwater photic environments has occurred through an increase of the number of opsin genes (Feuda et al, 2016;Liegertová et al, 2015).…”