Abstract
Lake Baikal is the deepest and one of the most ancient lakes in the world. Its unique ecology has resulted in the colonization of a diversity of depth habitats by a unique fauna that includes a group of teleost fish of the sub-order Cottoidei. This relatively recent radiation of cottoid fishes shows a gradual blue-shift in the wavelength of the absorption maximum of their visual pigments with increasing habitat depth. Here we combine homology modeling and quantum chemical calculations with experimental in vitro measurements of rhodopsins to investigate dim-light adaptation. The calculations, which were able to reproduce the trend of observed absorption maxima in both A1 and A2 rhodopsins, reveal a Barlow-type relationship between the absorption maxima and the thermal isomerization rate suggesting a link between the observed blue-shift and a thermal noise decrease. A Nakanishi point-charge analysis of the electrostatic effects of non-conserved and conserved amino acid residues surrounding the rhodopsin chromophore identified both close and distant sites affecting simultaneously spectral tuning and visual sensitivity. We propose that natural variation at these sites modulate both the thermal noise and spectral shifting in Baikal cottoid visual pigments resulting in adaptations that enable vision in deep water light environments.
Highlights
An alternative explanation for the λmax blue-shift observed in the deeper Baikal rhodopsins may be based on the existence of a Barlow-like correlation[9,10]
The results show that the amino acid substitutions found in the sequences of the selected Baikal rhodopsin set, modulate ΔE and EaT simultaneously in an interdependent parallel fashion suggesting that a reduction in thermal noise may have evolved in Lake Baikal fish pigments as a dim-light adaptation for increased photosensitivity
The sequence similarity and marked λmax variation of Baikal rhodopsins facilitate the study of the effect of single amino acid substitutions on ΔE and EaT
Summary
The same analysis indicates that, due to a cancellation of ΔE-ΔEoff of opposite signs (e.g. the sizable R140C red-shifting replacement is counterbalanced by the smaller T209I, L176S, T297S blue-shifting replacements in Fig. S6), the substitution of extra-cavity residues contributes only modestly to the λmax change from P. kneri to A. korotneffi. The loss of OH in position 261 in A. korotneffi, which used to form a hydrogen bond with the backbone oxygen of the conserved G121 residue in P. kneri (compare bottom and top in Fig. 3b), induces an HBN change This change affects the stability of the TS and S0 reactant differently and contributes to the EaT increase in A. korotneffi. Our implementation of Nakanishi’s point charge analysis has identified 8 rhodopsin substitutions, over a total of 20, modulating light sensitivity from red-shifted P. kneri to the blue-shifted A. korotneffi. Our results suggest that it is possible similar mechanisms may underlie colonization of other deepwater dimly lit environments such as those inhabited by deep sea fishes in marine habitats
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