Mechanisms of wavelength tuning in the rod opsins of deep-sea fishes

Abstract

SUMMARYThe main object of this study was to investigate the molecular basis for changes in the spectral sensitivity of the visual pigments of deep-sea fishes. The four teleost species studied, Hoplostethus mediterraneus, ataet x laticeps, Gonostoma elongatum and Histiobranchus bath bius, are phylogenetically distant from each other and live at depths ranging from 500 to almost 5000 m. A single fragment of the intronless rod opsin gene was PCR-amplified from each fish and sequenced. The wavelength of peak sensitivity for the rod visual pigments of the four deep-sea species varies from 483 nm in H. mediterraneus and G. elongatum to 468 nm in . laticeps. Six amino acids at sites on the inner face of the chromophore-binding pocket formed by the seven transmembrane a-helices are identified as candidates for spectral tuning. Substitutions at these sites involve either a change of charge, or a gain or loss of a hydroxyl group. Two of these, at positions 83 and 292, are consistently substituted in the visual pigments of all four species and are likely to be responsible for the shortwave sensitivity of the pigments. Shifts to wavelengths shorter than 480 nm may involve substitution at one or more of the remaining four sites. None of the modifications found in the derived sequences of these opsins suggest functional adaptations, such as increased content of hydroxyl-bearing or proline residues, to resist denaturation by the elevated hydrostatic pressures of the deep sea. Phylogenetic evidence for the duplication of the rod opsin gene in the Anguilliform lineage is presented.

Individual variation in rod absorbance spectra correlated with opsin gene polymorphism in sand goby (Pomatoschistus minutus)

“…In the dim and spectrally restricted illumination encountered even at moderate depths, maximizing quantum catch is imperative and sensitivity will depend even on small shifts of the visual pigment absorbance spectrum. Many studies have revealed spectral adaptations between different fish species (Hunt et al, 1996;Hunt et al, 2001;Hope et al, 1997;Carleton and Kocher, 2001;Parry et al, 2005;Carleton et al, 2005;Carleton et al, 2008;Seehausen et al, 2008). However, there has been little evidence on incipient evolutionary adaptation of rod spectral sensitivity between separated populations inhabiting spectrally different waters.…”

“…When going from marine to coastal, brackish or fresh water basins, the ambient light environments tends to shift from blue to green, yellow or even reddish brown, challenging the visual systems of the animals and creating a laboratory for studies on evolutionary adaptation of visual pigments (e.g. Hunt et al, 1996;Hunt et al, 2001;Hope et al, 1997;Yokoyama and Tada, 2000). The performance of rod vision is expected to depend in a straightforward manner on the degree of 'match' between the absorbance spectrum of the visual pigment and the illumination spectrum, because the visual information obtained at low light levels is critically dependent on photon catch, and rods alone convey information at these light levels.…”

Adaptive color vision in Pullosquilla litoralis (Stomatopoda,Lysiosquilloidea) associated with spectral and intensity changes in light environment

“…In most animals with varying spectral receptor classes, changes occur either on evolutionary time scales (Carleton and Kocher, 2001;Cronin et al, 1996;Hope et al, 1997;Hunt et al, 1996;Lythgoe et al, 1994;McDonald and Hawryshyn, 1995;Morris et al, 1993) or concurrent with overall ontogenetic changes in physiology (Beaudet and Hawryshyn, 1999;Cronin and Jinks, 2002;Shand, 1993;Shand et al, 1999). Visual changes resulting from chromophore replacement also occur in adult animals in response to changes in temperature and diurnal light (Cronin and Hariyama, 2002;Saszik and Bilotta, 1999;Suzuki et al, 1985;Tsin and Beatty, 1977).…”

Parallelism of amino acid changes at the RH1 affecting spectral sensitivity among deep-water cichlids from Lakes Tanganyika and Malawi

“…It is believed that the replacement A292S resulting in blue shifts of RH1 pigments has occurred several times during the 400 million years of vertebrate evolution (26,59,60). In the present study, however, we have demonstrated that the same replacement has occurred in cichlids over a very short evolutionary period of a few million years, although several amino acid positions are known to shift the max of RH1 pigment (26).…”