The visual pigments of a deep-sea teleost, the pearl eyeScopelarchus analis

Abstract

SUMMARY The eyes of deep-sea fish have evolved to function under vastly reduced light conditions compared to those that inhabit surface waters. This has led to a bathochromatic shift in the spectral location of maximum absorbance(λmax) of their rod (RH1) pigments and the loss of cone photoreceptors. There are exceptions to this, however, as demonstrated by the deep-sea pearl eye Scopelarchus analis. Here we show the presence of two RH1 pigments (termed RH1A and RH1B) and a cone RH2 pigment. This is therefore the first time that the presence of a cone pigment in a deep-sea fish has been confirmed by molecular analysis. The λmaxvalues of the RH1A and RH1B pigments at 486 and 479 nm, respectively, have been determined by in vitro expression of the recombinant opsins and show the typical short-wave shifts of fish that live in deep water compared to surface dwellers. RH1B, however, is expressed only in more adult fish and lacks key residues for phosphorylation, indicating that it may not be involved in image formation. In contrast, the RH2 pigment has additional residues near the C terminus that may be involved in phosphorylation and does not show temporal changes in expression. The distribution of these pigments within the multiple retinae of S. analis is discussed.

A second visual rhodopsin gene,rh1-2, is expressed in zebrafish photoreceptors and found in other ray-finned fishes

“…This switch of both opsin and chromophore is a clear example of an adjustment of the visual system as a result of a change in photic environment. Another example is the deep-sea pearleye, S. analis, which has a more traditional rh1A gene, along with rh1B, expressed alongside rh1A in adult fish living over 900 m below the surface (Pointer et al, 2007). The pearleye has unique cylindrical eye morphology, containing both a main retina, used for image formation, and an accessory retina, likely only capable of gross light perception (Collin et al, 1998), with rh1B expression being localized in this accessory retina (Pointer et al, 2007).…”

“…Another example is the deep-sea pearleye, S. analis, which has a more traditional rh1A gene, along with rh1B, expressed alongside rh1A in adult fish living over 900 m below the surface (Pointer et al, 2007). The pearleye has unique cylindrical eye morphology, containing both a main retina, used for image formation, and an accessory retina, likely only capable of gross light perception (Collin et al, 1998), with rh1B expression being localized in this accessory retina (Pointer et al, 2007). Zebrafish do not experience an ontogenetic migration, possess only A1 chromophore-based visual pigments (Allison et al, 2004), do not occupy deep-sea habitats and do not have abnormal eye or retinal morphology, suggesting that it is unlikely that rh1-2 serves a similar function to the duplicated rhodopsin genes in either eels or the pearleye.…”

“…Several eel species have two rhodopsins, one freshwater (rh1fwo) and one marine (rh1dso), and expression shifts from the former to the latter following migration during maturation (Beatty, 1975;Hope et al, 1998;Zhang et al, 2000;Zhang et al, 2002). The short-fin pearleye (Scopelarchus analis), a deep-sea teleost, also expresses an additional rh1 gene, rh1b, in the accessory retina of adult fish after descending to greater ocean depths (Pointer et al, 2007). Other examples of multiple rh1 genes are usually the result of species-specific duplication events (Lim et al, 1997).…”

Spectral Tuning in the Eyes of Deep-Sea Lanternfishes (Myctophidae): A Novel Sexually Dimorphic Intra-Ocular Filter

“…However, analysis of the rod opsin coding sequences expressed in S. evermanni revealed the presence of 2 Rh1 opsin genes ( . This is only the second case of a rod opsin duplication recorded for a deep-sea fish, the first being the pearleye S. analis [Pointer et al, 2007]. However, in contrast to S. analis, for which the duplication of Rh1 results in 2 spectrally similar visual pigments (486 and 479 nm [Pointer et al, 2007]), duplication in S. evermanni gives rise to 2 spectrally distinct visual pigments, with peaks at 476 and 503 nm.…”

“…This is only the second case of a rod opsin duplication recorded for a deep-sea fish, the first being the pearleye S. analis [Pointer et al, 2007]. However, in contrast to S. analis, for which the duplication of Rh1 results in 2 spectrally similar visual pigments (486 and 479 nm [Pointer et al, 2007]), duplication in S. evermanni gives rise to 2 spectrally distinct visual pigments, with peaks at 476 and 503 nm. Moreover, while the 2 Rh1 genes are phylogenetically different in S. analis, indicating an early duplication in evolutionary history [Pointer et al, 2007], the Rh1-A and Rh1-B genes in S. evermanni are phylogenetically very similar, indicating the origin of the duplication within a clade defined by 3 genera of myctophids .…”