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Vision using multiple distinct rod opsins in deep-sea fishes

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Science  10 May 2019:
Vol. 364, Issue 6440, pp. 588-592
DOI: 10.1126/science.aav4632
  • Fig. 1 Diversity of visual opsin genes in teleost fishes.

    The time-calibrated phylogeny in the center is based on molecular information from 101 fish genomes and is shaded according to the median depth of occurrence of each species (terminal branches) and reconstructed depths (internal branches). Colored bars in the outer circles indicate the number of cone opsin genes, black bars represent the number of rod opsins (RH1s), and dotted bars denote incomplete or ambiguous data. Deep-sea lineages with multiple RH1 copies are highlighted with dashed boxes. A detailed version of the phylogeny, including full species names, is provided in fig. S1.

  • Fig. 2 Molecular function of rod photoreceptors in the silver spinyfin.

    (A) Expression of RH1 genes in the retina of epipelagic larvae (upper panel) and adults (lower panel). (B) Peak spectral sensitivities (λmax) of 37 (out of 38) RH1s of D. argenteus on the basis of in vitro protein regenerations (black) and subsequent key tuning-site predictions (gray). (C) Reconstruction of mean subclade disparity through time in λmax values for the RH1s of D. argenteus, supporting an early-burst (EB) scenario of diversification (Akaike information criterion AICEB = 236.4) over time-homogeneous diversification [Brownian motion (BM); AICBM = 244.9] or selection toward an optimal value of λmax [Ornstein-Uhlenbeck model (OU), not shown; AICOU = 246.9]. Ma, million years. (D) Functional divergence through time of λmax values according to predicted λmax values for reconstructed ancestral sequences (black) and ancestral λmax values reconstructed on the basis of an EB model (gray).

  • Fig. 3 Evolution and functional diversification of RH1 in deep-sea fishes.

    (A) Time-calibrated gene tree based on teleost RH1s, demonstrating lineage-specific duplications in three deep-sea fish lineages. Vertical bars indicate amino acid substitutions in key spectral tuning sites (1, 3). Asterisks denote gene duplication events. The branches in the gene tree are color-coded according to the rate of nonsynonymous to synonymous substitutions (dN/dS); each branch’s thickness corresponds to the reconstructed substitution rate. (B) Distribution of the per-branch dN/dS values within the RH1s of Diretmidae compared with that of all other branches in the teleost RH1 gene tree, based on ancestral sequence reconstructions. (C) Basic model of the RH1 protein showing its seven transmembrane helices and the positions of known key spectral tuning sites, including the disulfide bridge reported here.

Supplementary Materials

  • Vision using multiple distinct rod opsins in deep-sea fishes

    Zuzana Musilova, Fabio Cortesi, Michael Matschiner, Wayne I. L. Davies, Jagdish Suresh Patel, Sara M. Stieb, Fanny de Busserolles, Martin Malmstrøm, Ole K. Tørresen, Celeste J. Brown, Jessica K. Mountford, Reinhold Hanel, Deborah L. Stenkamp, Kjetill S. Jakobsen, Karen L. Carleton, Sissel Jentoft, Justin Marshall, Walter Salzburger

    Materials/Methods, Supplementary Text, Tables, Figures, and/or References

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    • Materials and Methods
    • Supplementary Text
    • Figs. S1 to S10
    • Tables S1 to S11
    • Captions for Movies S1 and S2
    • References

    Images, Video, and Other Media

    Movie S1
    100 ns molecular dynamics simulation of Rh1_Lc pigment (λmax=504 nm) in an explicit bilayer and water. Green, protein; red, chromophore+lysine; magenta, palmitoyl moiety; white (near chromophore binding pocket), disulfide bridge; small blue spheres, water molecules. Phospholipids: silver, carbon atoms; yellow, phosphorus atoms; purple, head group nitrogen.
    Movie S2
    100 ns molecular dynamics simulation of Rh1_Fb pigment (λmax=449 nm) in an explicit bilayer and water. Purple, protein; red, chromophore+lysine; magenta, palmitoyl moiety; small blue spheres, water molecules. Phospholipids: silver, carbon atoms; yellow, phosphorus atoms; purple, head group nitrogen.

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