Abstract
The spectral composition of ambient light varies across both space and time. Many species of jawed vertebrates adapt to this variation by tuning the sensitivity of their photoreceptors via the expression of CYP27C1, an enzyme that converts vitamin A1 into vitamin A2, thereby shifting the ratio of vitamin A1-based rhodopsin to red-shifted vitamin A2-based porphyropsin in the eye. Here, we show that the sea lamprey (Petromyzon marinus), a jawless vertebrate that diverged from jawed vertebrates during the Cambrian period (approx. 500 Ma), dynamically shifts its photoreceptor spectral sensitivity via vitamin A1-to-A2 chromophore exchange as it transitions between photically divergent aquatic habitats. We further show that this shift correlates with high-level expression of the lamprey orthologue of CYP27C1, specifically in the retinal pigment epithelium as in jawed vertebrates. Our results suggest that the CYP27C1-mediated vitamin A1-to-A2 switch is an evolutionarily ancient mechanism of sensory plasticity that appeared not long after the origin of vertebrates.
Highlights
Variability in the intensity and spectral composition of light in the natural world presents fundamental challenges for vision, and many features of the vertebrate eye are adaptations to meet these challenges
To confirm that this population maintains the A1-to-A2 switch, we analysed the retinoid content of the eyes of juvenile and adult lamprey with high-performance liquid chromatography (HPLC)
Consistent with earlier studies of lamprey visual pigments [16,17], we found that this red-shift is attributable to a switch in the visual pigment chromophore from 11-cis retinal (A1) to 11-cis 3,4-didehydroretinal (A2)
Summary
Variability in the intensity and spectral composition of light in the natural world presents fundamental challenges for vision, and many features of the vertebrate eye are adaptations to meet these challenges. In some aquatic environments such as ponds, streams and rivers, specific wavelengths of light are scattered or absorbed by sediment and dissolved organic matter, resulting in a marked shift in the spectral composition of light towards longer wavelengths [1,2]. A wide variety of aquatic organisms optimize visual sensitivity and discrimination by matching the sensitivities of their photoreceptors to the available light spectrum [2,3,4,5]. To maintain this match, as light environments change over space and time, many species have evolved mechanisms of visual system plasticity: that allow them to shift photoreceptor sensitivity dynamically. We focus on another widespread mechanism of visual system plasticity: the ‘rhodopsin–porphyropsin’ switch [8]
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