Rhodopsin in the Dark Hot Sea: Molecular Analysis of Rhodopsin in a Snailfish, Careproctus rhodomelas, Living near the Deep-Sea Hydrothermal Vent.

Rie Sakata,Hiromasa Mitsui,Hiroyuki Yamamoto,Ryo Kabutomori,Tetsuya Miwa,Toshiyuki Okano,Keiko Okano,Akihiro Takemura,Wayne Iwan Lee Davies

doi:10.1371/journal.pone.0135888

Rie Sakata, Hiromasa Mitsui + Show 7 more

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https://doi.org/10.1371/journal.pone.0135888

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Abstract

Visual systems in deep-sea fishes have been previously studied from a photobiological aspect; however, those of deep-sea fish inhabiting the hydrothermal vents are far less understood due to sampling difficulties. In this study, we analyzed the visual pigment of a deep-sea snailfish, Careproctus rhodomelas, discovered and collected only near the hydrothermal vents of oceans around Japan. Proteins were solubilized from the C. rhodomelas eyeball and subjected to spectroscopic analysis, which revealed the presence of a pigment characterized by an absorption maximum (λmax) at 480 nm. Immunoblot analysis of the ocular protein showed a rhodopsin-like immunoreactivity. We also isolated a retinal cDNA encoding the entire coding sequence of putative C. rhodomelas rhodopsin (CrRh). HEK293EBNA cells were transfected with the CrRh cDNA and the proteins extracted from the cells were subjected to spectroscopic analysis. The recombinant CrRh showed the absorption maximum at 480 nm in the presence of 11-cis retinal. Comparison of the results from the eyeball extract and the recombinant CrRh strongly suggests that CrRh has an A1-based 11-cis-retinal chromophore and works as a photoreceptor in the C. rhodomelas retina, and hence that C. rhodomelas responds to dim blue light much the same as other deep-sea fishes. Because hydrothermal vent is a huge supply of viable food, C. rhodomelas likely do not need to participate diel vertical migration and may recognize the bioluminescence produced by aquatic animals living near the hydrothermal vents.

Highlights

Photoreceptors in rods and cones are comprised of rhodopsins and cone visual pigments, and these visual pigments are composed of apoprotein and 11-cis-retinal chromophore
The dive expedition for sampling using a remotelyoperated vehicle (ROV) Hyper-Dolphin equipped with Deep Aquarium system, which is a sampling tool to hold in situ condition during operation, was conducted in a research cruise (NT08-15) of R/V Natsushima [22]
The extract obtained from eyeball of C. rhodomelas (Fig 1A) was subjected to photospectroscopic analysis and the absolute absorption spectrum showed the presence of component(s) with absorption around 410 nm and 480 nm (Fig 1B, "eyeball extract")

Summary

Introduction

Photoreceptors in rods and cones are comprised of rhodopsins and cone visual pigments, and these visual pigments are composed of apoprotein (opsin) and 11-cis-retinal chromophore. Rods are more sensitive to light than cones, but the light response of rods is slower than that of cones [1]. The deep ocean is a unique photic environment because of the extraordinarily low light levels present, which places different evolutionary constraints on the visual system of deep-sea fish. There are two main natural sources of illumination in the deep sea: residual sunlight and bioluminescence. The second source of light in the deep sea is the bioluminescence produced by the aquatic animals themselves, whose peak emission is usually around the same wavelengths as the remaining sunlight [6, 7]

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