Animal opsins support vision throughout the animal kingdom. They are members of the G protein coupled receptor (GPCR) superfamily and as such exist in hepta-helical arrangements in the membranes of photoreceptor cells. They transduce light energy into biochemical energy via binding of an exogenous chromophore, retinaldehyde, which isomerizes in response to light, initiating conformational rearrangements of the transmembrane helices and G protein binding. Four main opsin families exist; the ciliary-type, rhabdomeric-type, ‘group 4' opsins and the most recently discovered cnidopsin group. Little is know about the structure, function and diversity of opsins within this latter group, which exists in animals, cnidarians, distantly related to the vast majority of animal species. Jellyfish opsin (JellyOp) is the only cnidopsin to be studied in any detail to date. Isolated from the lens eyes of the visually adept box jellyfish C.Rastonii, it couples to the Gs-cAMP signaling pathway. This signaling pathway is utilised by human dopaminergic and serotenergic receptors, which has lead to employment of JellyOp as an optogenetic tool for light controlled cAMP induction in vitro. Here I set out to perform the first structural investigation of a cnidarian opsin, using JellyOp, to both further understanding of cnidarian opsin structure and function, but also test hypotheses to improve JellyOp as an optogenetic tool. In chapter 3, I used a combination of homology modeling, ultraviolet (UV)-visible light spectroscopy and 2nd messenger assays to identify a novel counterion position in JellyOp (E94 in TM2). This is only the third counterion position discovered in animal opsins and shows a parallel shift in tertiary structure as is seen in the vertebrate ciliary opsins, suggesting this may be an instance of convergent evolution between distantly related proteins. Furthermore we were able to validate a evolutionary path between the now three counterion phenotypes (E94/E113/E181) by either removing a conserved positive charge, R186, in JellyOp's second extracellular loop or substituting JellyOp's counterion for the vertebrate counterion at position 113. In chapter 4, I employed the homology model of JellyOp's retinal binding pocket to design novel spectral tuning mutations to red shift JellyOp's spectral sensitivity for improved optogenetic versatility. We show that the OH- site rule, determined in vertebrate cone opsins, can be applied to JellyOp to achieve individual red shifts of up to 19nm. The magnitude of red shift correlates with the distance of the newly introduced hydroxyl group and the retinal chain, but also with significantly perturbed opsin function. We find that adding these mutations together either produce sub-additive spectral shifts or render the protein non functional, limiting the application of this method for effective optogenetic tool development. In chapter 5 I used the unique screen for counterion neutralisation developed in chapter 3 to attempt to identify the counterion of human melanopsin. Melanopsin is a mammalian opsin involved in entraining circadian rhythms and the pupillary light reflex, but to date has had little structural information resolved. I started by revealing the counterion-neutralized phenotype of human rhodopsin (E113Q) in HEK293 cells for the first time. However, our assay was then unable to detect any change in spectral sensitivity indicative of counterion neutralisation in four mutants targeted to three acidic residues in human melanopsin's sequence. This indicated that in our conditions the schiff base remained fully protonated in lieu of a counterion or that we were unable to correctly identify melanopsin's counterion position.