Cambrian origin of the CYP27C1-mediated vitamin A ₁ -to-A ₂ switch, a key mechanism of vertebrate sensory plasticity

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.

A death in the family: Sea lamprey (Petromyzon marinus) avoidance of confamilial alarm cues diminishes with phylogenetic distance

“…Discharge was maintained between 9 and 10 L/s. Although adult sea lamprey can perceive long wavelength light (Morshedian et al., ), infrared lamps do not alter their natural behavioral tendencies in captivity. Therefore, both experimental arenas were monitored by infrared‐sensitive video cameras (Axis Communications; Q1604 Network Camera) positioned above the center of the arena, in conjunction with two infrared lights (Wildlife Engineering; Model IRLamp6).…”

Seeing the rainbow: mechanisms underlying spectral sensitivity in teleost fishes

“…This suggests that these mechanisms arose early in vertebrate evolution; indeed, this idea is well supported by studies of migrating lamprey. This basal vertebrate has the ability to switch chromophore, gene expression and even ellipsosomes through ontogeny (Collin et al, 2003a;Davies et al, 2007;Morshedian et al, 2017). Comparisons between lamprey species also show evidence of opsin gene loss (Davies et al, 2009).…”

Light adaptation and the evolution of vertebrate photoreceptors

“…Cells were stimulated with a dual-beam optical bench; the light of halogen lamp bulbs was passed through electronic shutters (Uniblitz, Vincent Associates, Rochester, NY, USA) and interference filters at wavelengths of 500 nm for rods and 600 nm for cones, near the peaks of spectral sensitivities of both receptors (Morshedian et al 2017). The intensity of the light was attenuated with absorptive neutral-density filters.…”

“…The light intensity was calibrated with a photodiode (UDT Instruments, San Diego, CA, USA, formerly Graseby Optronics). Because there is some uncertainty about photoreceptor dimensions and the specific absorbance of lamprey photoreceptor pigments (Hárosi & Kleinschmidt, 1993;Morshedian et al 2017), we calculated intensities in units of rhodopsins bleached (Rh * ) from the dark-adapted response-intensity curve (Fig. 3A) and the amplitude of the single-photon response of lamprey rods (Morshedian & Fain, 2015).…”

“…6). From the specific optical density of rod pigment of 0.005-0.01 μm −1 (Hárosi & Kleinschmidt, 1993;Morshedian et al 2017) and the rod dimensions (Dickson & Graves, 1979;Hárosi & Kleinschmidt, 1993), there are about 2-4 × 10 8 pigment molecules in a lamprey rod, half as opsin at steady state after a 50% bleach. Bleached pigment is therefore about 1-3 × 10 −6 times as effective at stimulating the cascade as real light.…”