Spectral tuning and deactivation kinetics of marine mammal melanopsins.

Jeffry I Fasick,Lorian E Schweikert,Padmanabhan Mahadevan,Haya Algrain,Courtland Samuels,Phyllis R Robinson,Zaid J Naffaa,Stephan C.F Neuhauss

doi:10.1371/journal.pone.0257436

Abstract

In mammals, the photopigment melanopsin (Opn4) is found in a subset of retinal ganglion cells that serve light detection for circadian photoentrainment and pupil constriction (i.e., mydriasis). For a given species, the efficiency of photoentrainment and length of time that mydriasis occurs is determined by the spectral sensitivity and deactivation kinetics of melanopsin, respectively, and to date, neither of these properties have been described in marine mammals. Previous work has indicated that the absorbance maxima (λmax) of marine mammal rhodopsins (Rh1) have diversified to match the available light spectra at foraging depths. However, similar to the melanopsin λmax of terrestrial mammals (~480 nm), the melanopsins of marine mammals may be conserved, with λmax values tuned to the spectrum of solar irradiance at the water's surface. Here, we investigated the Opn4 pigments of 17 marine mammal species inhabiting diverse photic environments including the Infraorder Cetacea, as well as the Orders Sirenia and Carnivora. Both genomic and cDNA sequences were used to deduce amino acid sequences to identify substitutions most likely involved in spectral tuning and deactivation kinetics of the Opn4 pigments. Our results show that there appears to be no amino acid substitutions in marine mammal Opn4 opsins that would result in any significant change in λmax values relative to their terrestrial counterparts. We also found some marine mammal species to lack several phosphorylation sites in the carboxyl terminal domain of their Opn4 pigments that result in significantly slower deactivation kinetics, and thus longer mydriasis, compared to terrestrial controls. This finding was restricted to cetacean species previously found to lack cone photoreceptor opsins, a condition known as rod monochromacy. These results suggest that the rod monochromat whales rely on extended pupillary constriction to prevent photobleaching of the highly photosensitive all-rod retina when moving between photopic and scotopic conditions.

Highlights

The vertebrate visual system evolved to detect light for both image forming vision and nonimage forming processes, and emerged approximately 500 million years ago [1]
We hypothesized that marine mammal melanopsins possess few if any amino acid substitutions that would result in a deviation from the absorbance maxima of typical terrestrial mammalian melanopsins (~480 nm)
This study addressed two principal questions pertaining to marine mammal melanopsins regarding the spectral tuning properties of the pigments and the role that melanopsin plays in the pupillary light reflex (PLR)

Summary

Introduction

The vertebrate visual system evolved to detect light for both image forming vision and nonimage forming processes, and emerged approximately 500 million years ago [1]. Marine mammals have undergone a variety of adaptations to their visual systems upon their return to the sea These mammals, which include the orders Cetacea, Sirenia, and Carnivora which includes pinnipeds (Otariidae, Phocidae, Odobenidae), polar bears (Ursidae) and sea otters (Mustelidae), possess eyes that, for most species, have been modified to enhance image formation underwater. Most marine mammals possess both functional rod and LWS cone photoreceptors, only Sirenia, Ursidae and Mustelidae possess both LWS and SWS1 cone photoreceptors allowing for dichromatic color vision [9, 10]. All cetacean and pinniped species have lost functional SWS1 cone photoreceptors resulting in the loss of typical dichromatic color vision [3, 7, 8, 11,12,13,14,15,16,17]. Almost all baleen and beaked whale species have lost the LWS cone visual pigment resulting in rod monochromacy [7] while retaining the LWS cone soma and maintenance of rod/cone based retinal circuitry [8]

Methods

Results

Conclusion