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Molecular diversity of visual pigments in Stomatopoda (Crustacea)

Published online by Cambridge University Press:  01 May 2009

MEGAN L. PORTER ,
MICHAEL J. BOK ,
PHYLLIS R. ROBINSON  and
THOMAS W. CRONIN
MEGAN L. PORTER*
Affiliation:
Department of Biological Sciences, University of Maryland, Baltimore County, Baltimore, Maryland
MICHAEL J. BOK
Affiliation:
Department of Biological Sciences, University of Maryland, Baltimore County, Baltimore, Maryland
PHYLLIS R. ROBINSON
Affiliation:
Department of Biological Sciences, University of Maryland, Baltimore County, Baltimore, Maryland
THOMAS W. CRONIN
Affiliation:
Department of Biological Sciences, University of Maryland, Baltimore County, Baltimore, Maryland
*
*Address correspondence and reprint requests to: Megan L. Porter, Department of Biological Sciences, University of Maryland, Baltimore County, Baltimore, MD 21250. E-mail: porter@umbc.edu
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Abstract

Stomatopod crustaceans possess apposition compound eyes that contain more photoreceptor types than any other animal described. While the anatomy and physiology of this complexity have been studied for more than two decades, few studies have investigated the molecular aspects underlying the stomatopod visual complexity. Based on previous studies of the structure and function of the different types of photoreceptors, stomatopod retinas are hypothesized to contain up to 16 different visual pigments, with 6 of these having sensitivity to middle or long wavelengths of light. We investigated stomatopod middle- and long-wavelength-sensitive opsin genes from five species with the hypothesis that each species investigated would express up to six different opsin genes. In order to understand the evolution of this class of stomatopod opsins, we examined the complement of expressed transcripts in the retinas of species representing a broad taxonomic range (four families and three superfamilies). A total of 54 unique retinal opsins were isolated, resulting in 6–15 different expressed transcripts in each species. Phylogenetically, these transcripts form six distinct clades, grouping with other crustacean opsins and sister to insect long-wavelength visual pigments. Within these stomatopod opsin groups, intra- and interspecific clusters of highly similar transcripts suggest that there has been rampant recent gene duplication. Some of the observed molecular diversity is also due to ancient gene duplication events within the stem crustacean lineage. Using evolutionary trace analysis, 10 amino acid sites were identified as functionally divergent among the six stomatopod opsin clades. These sites form tight clusters in two regions of the opsin protein known to be functionally important: six in the chromophore-binding pocket and four at the cytoplasmic surface in loops II and III. These two clusters of sites indicate that stomatopod opsins have diverged with respect to both spectral tuning and signal transduction.

Keywords

StomatopodaOpsinVisual pigmentMolecular evolution
Type
Research Articles
Information
Visual Neuroscience , Volume 26 , Issue 3 , May 2009 , pp. 255 - 265
Copyright
Copyright © Cambridge University Press 2009

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References

Abascal, F., Zardoya, R. & Posada, D. (2005). ProtTest: Selection of best-fit models of protein evolution. Bioinformatics 21, 2104–2105.Google Scholar
Ahyong, S.T. & Harling, C. (2000). The phylogeny of the stomatopod Crustacea. Australian Journal of Zoology 48, 607–642.Google Scholar
Altenbach, C., Yang, K., Farrens, D.L., Farahbakhsh, Z.T., Khorana, H.G. & Hubbell, W.L. (1996). Structural features and light-dependent changes in the cytoplasmic interhelical EF loop region of rhodopsin: A site-directed spin-labeling study. Biochemistry 35, 12470–12478.Google Scholar
Bates, P.A., Kelley, L.A., MacCallum, R.M. & Sternberg, M.J.E. (2001). Enhancement of protein modeling by human intervention in applying the automatic programs 3D-Jigsaw and 3D-Pssm. Proteins: Structure, Function and Genetics 45(Suppl. 5), 39–46.Google Scholar
Bates, P.A. & Sternberg, M.J.E. (1999). Model building by comparison at Casp3: Using expert knowledge and computer automation. Proteins: Structure, Function and Genetics 37(Suppl. 3), 47–54.Google Scholar
Borjigin, J. & Nathans, J. (1994). Insertional mutagenesis as a probe of rhodopsin’s topography, stability, and activity. The Journal of Biological Chemistry 269, 14715–14722.Google Scholar
Bowmaker, J.K. & Hunt, D.M. (2006). Evolution of vertebrate visual pigments. Current Biology 16, R484–R489.Google Scholar
Bradley, R.D. & Hillis, D.M. (1997). Recombinant DNA sequences generated by PCR amplification. Molecular Biology and Evolution 14, 592–593.Google Scholar
Briscoe, A.D. (2001). Functional diversification of lepidopteran opsins following gene duplication. Molecular Biology and Evolution 18, 2270–2279.Google Scholar
Briscoe, A.D. & Chittka, L. (2001). The evolution of color vision in insects. Annual Review of Entomology 46, 471–510.Google Scholar
Brown, A.J.H. (1996). Isolation and Characterisation of Visual Pigment Genes From the Stomatopod Crustacean Gonodactylus oerstedii. University of Sussex: Susson, UK.Google Scholar
Carleton, K.L., Spady, T.C. & Cote, R.H. (2005). Rod and cone opsin families differ in spectral tuning domains but not signal transducing domains as judged by saturated evolutionary trace analysis. Journal of Molecular Evolution 61, 75–89.Google Scholar
Chiao, C.C., Cronin, T.W. & Marshall, N.J. (2000). Eye Design and Color Signaling in a Stomatopod Crustacean Gonodactylus smithii. Brain, Behavior and Evolution 56, 107–122.Google Scholar
Contreras-Moreira, B. & Bates, P.A. (2002). Domain fishing: A first step in protein comparative modelling. Bioinformatics 18, 1141–1142.Google Scholar
Cowing, J.A., Poopalasundaram, S., Wilkie, S.E., Robinson, P.R., Bowmaker, J.K. & Hunt, D.M. (2002). The molecular mechanism for the spectral shifts between vertebrate ultraviolet-and violet-sensitive cone visual pigments. Biochemical Journal 367, 129–135.Google Scholar
Cronin, T.W. (1985). The visual pigment of a stomatopod crustacean, Squilla empusa. Journal of Comparative Physiology A 156, 679–687.Google Scholar
Cronin, T.W. & Marshall, N.J. (1989 a). A retina with at least ten spectral types of photoreceptors in a mantis shrimp. Nature 339, 137–140.Google Scholar
Cronin, T.W. & Marshall, N.J. (1989 b). Multiple spectral classes of photoreceptors in the retinas of gonodactyloid stomatopod crustaceans. Journal of Comparative Physiology A: Sensory, Neural, and Behavioral Physiology 166, 261–275.Google Scholar
Cronin, T.W., Marshall, N.J. & Caldwell, R.L. (1993). Photoreceptor spectral diversity in the retinas of squilloid and lysiosquilloid stomatopod crustaceans. Journal of Comparative Physiology A: Sensory, Neural, and Behavioral Physiology 172, 339–350.Google Scholar
Cronin, T.W., Marshall, N.J. & Caldwell, R.L. (1994). The retinas of mantis shrimps from low-light environments (Crustacea; Stomatopoda; Gonodactylidae). Journal of Comparative Physiology A: Sensory, Neural, and Behavioral Physiology 174, 607–619.Google Scholar
Cronin, T.W., Marshall, N.J. & Caldwell, R.L. (1996). Visual pigment diversity in two genera of mantis shrimps implies rapied evolution (Crustacea: Stomatopoda). Journal of Comparative Physiology A 179, 371–384.Google Scholar
Cronin, T.W. & Jinks, R.N. (2001). Ontogeny of Vision in Marine Crustaceans. American Zoologist 41, 1098–1107.Google Scholar
Cronin, T.W. & Marshall, N.J. (2004). The unique visual world of mantis shrimp. In Complex Worlds From Simple Nervous Systems, ed. Prete, F., pp. 239–268. Cambridge, MA: MIT Press.Google Scholar
Cronin, T.W., Marshall, N.J. & Caldwell, R.L. (2000). Spectral tuning and the visual ecology of mantis shrimps. Philosophical Transactions of the Royal Society Series B 355, 1263–1267.Google Scholar
Do, C.B., Mahabhashyam, M.S.P, Brudno, M. & Batzoglou, S. (2005). Probcons: Probabilistic consistency-based multiple sequence alignment. Genome Research 15, 330–340.Google Scholar
Fasick, J.I., Applebury, M.L. & Oprian, D.D. (2002). Spectral tuning in the mammalian shortwavelength sensitive cone pigments. Biochemistry 41, 6860–6865.Google Scholar
Frank, T.M., Porter, M.L. & Cronin, T.W. (2009). Spectral sensitivity, visual pigments and screening pigments in two life history stages of the ontogenetic migrator Gnathophausia ingens. Journal of the Marine Biological Association of the United Kingdom, 89, 119–129 doi: 10.1017/Soo25315408002440.Google Scholar
Franke, R.R., Konig, B., Sakmar, T.P., Khorana, H.G. & Hofmann, K.P. (1990). Rhodopsin mutants that bind but fail to activate transducin. Science 250, 123.Google Scholar
Franke, R.R., Sakmar, T.P., Graham, R.M. & Khorana, H.G. (1992). Structure and function in rhodopsin. Studies of the interaction between the rhodopsin cytoplasmic domain and transducin. The Journal of Biological Chemistry 267, 14767–14774.Google Scholar
Frentiu, F.D., Bernard, G.D., Cuevas, C.I., Sison-Mangus, M.P., Prudic, K.L. & Briscoe, A.D. (2007 a). Adaptive evolution of color vision as seen through the eyes of butterflies. Proceedings of the National Academy of Sciences of the United States of America 104, 8634–8640.Google Scholar
Frentiu, F.D., Bernard, G.D., Sison-Mangus, M.P., Brower, A.V. & Briscoe, A.D. (2007 b). Gene duplication is an evolutionary mechanism for expanding spectral diversity in the long-wavelength photopigments of butterflies. Molecular Biology and Evolution 24, 2016–2028.Google Scholar
Guex, N. & Peitsch, M.C. (1997). Swiss-model and the Swiss-Pdb Viewer: An environment for comparative protein modeling. Electrophoresis 18, 2714–2723.Google Scholar
Guindon, S. & Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696–704.Google Scholar
Guindon, S., Lethiec, F., Duroux, P. & Gascuel, O. (2005). Phyml online—A web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Research 33, W557–W559.Google Scholar
Hill, C.A., Fox, A.N., Pitts, R.J., Kent, L.B., Tan, P.L., Chrystal, M.A., Cravchik, A., Collins, F.H., Robertson, H.M. & Zwiebel, L.J. (2002). G protein-coupled receptors in Anopheles gambiae. Science 298, 176–178.Google Scholar
Hillis, D.M. & Bull, J.J. (1993). An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Systematic Biology 42, 182–192.Google Scholar
Huber, T., Faulkner, G. & Hugenholtz, P. (2004). Bellerophon: A program to detect chimeric sequences in multiple sequence alignments. Bioinformatics 20, 2317–2319.Google Scholar
Janz, J.M. & Farrens, D.L. (2001). Engineering a functional blue-wavelength-shifted rhodopsin mutant. Biochemistry 40, 7219–7227.Google Scholar
Konig, B., Arendt, A., McDowell, J.H., Kahlert, M., Hargrave, P.A. & Hofmann, K.P. (1989). Three cytoplasmic loops of rhodopsin interact with transducin. Proceedings of the National Academy of Sciences of the United States of America 86, 6878–6882.Google Scholar
Koyanagi, M., Takano, K., Tsukamoto, H., Ohtsu, K., Tokunaga, F. & Terakita, A. (2008). Jellyfish vision starts with cAMP signaling mediated by opsin-G(s) cascade. Proceedings of the National Academy of Sciences of the United States of America 105, 15576–15580.Google Scholar
Landin, J.S., Katragadda, M. & Albert, A.D. (2001). Thermal destabilization of rhodopsin and opsin by proteolytic cleavage in bovine rod outer segment disk membranes. Biochemistry 40, 11176–11183.Google Scholar
Liang, Y., Fotiadis, D., Filipek, S., Saperstein, D.A., Palczewski, K. & Engel, A. (2003). Organization of the G protein-coupled receptors rhodopsin and opsin in native membranes. The Journal of Biological Chemistry 278, 21655–21662.Google Scholar
Lichtarge, O., Bourne, H.R. & Cohen, F.E. (1996). An evolutionary trace method defines binding surfaces common to protein families. Journal of Molecular Biology 257, 342–358.Google Scholar
Madabushi, S., Gross, A.K., Philippi, A., Meng, E.C., Wensel, T.G. & Lichtarge, O. (2004). Evolutionary trace of G protein-coupled receptors reveals clusters of residues that determine global and class-specific functions. The Journal of Biological Chemistry 279, 8126–8132.Google Scholar
Morris, A., Bowmaker, J.K. & Hunt, D.M. (1993). The molecular basis of a spectral shift in the rhodopsins of two species of squid from different photic environments. Proceedings of the Royal Society B: Biological Sciences 254, 233–240.Google Scholar
Murakami, M. & Kouyama, T. (2008). Crystal structure of squid rhodopsin. Nature 453, 363–367.Google Scholar
Nagata, T., Oura, T., Terakita, A., Kandori, H. & Shichida, Y. (2002). Isomer-Specific Interaction of the Retinal Chromophore with Threonine-118 in Rhodopsin. Journal of Physical Chemistry A 106, 1969–1975.Google Scholar
Nathans, J. (1990). Determinants of visual pigment absorbance: identification of the retinyidene Schiff's base counterion in bovine rhodopsin. Biochemistry 29, 9746–9752.Google Scholar
Natochin, M., Gasimov, K.G., Moussaif, M. & Artemyev, N.O. (2003). Rhodopsin determinants for transducin activation: A gain-of-function approach. The Journal of Biological Chemistry 278, 37574–37581.Google Scholar
Oakley, T.H. & Huber, D.R. (2004). Differential expression of duplicated opsin genes in two eye types of ostracod crustaceans. Journal of Molecular Evolution 59, 239–249.Google Scholar
Palczewski, K., Buczylko, J., Kaplan, M.W., Polans, A.S. & Crabb, J.W. (1991). Mechanism of rhodopsin kinase activation. The Journal of Biological Chemistry 266, 12949–12955.Google Scholar
Porter, M.L., Cronin, T.W., McClellan, D.A. & Crandall, K.A. (2007). Molecular characterization of crustacean visual pigments and the evolution of pancrustacean opsins. Molecular Biology and Evolution 24, 253–268.Google Scholar
Qiu, X., Wu, L., Huang, H., McDonel, P.E., Palumbo, A.V., Tiedje, J.M. & Zhou, J. (2001). Evaluation of PCR-generated chimeras, mutations, and heteroduplexes with 16S rRNA gene-based cloning. Applied and Environmental Microbiology 67, 880–887.Google Scholar
Ridge, K.D., Ngo, T., Lee, S.S.J. & Abdulaev, N.G. (1999). Folding and assembly in rhodopsin: Effect of mutations in the sixth transmembrane helix on the conformation of the third cytoplasmic loop. The Journal of Biological Chemistry 274, 21437–21442.Google Scholar
Sakamoto, K., Hisatomi, O., Tokunaga, F. & Eguchi, E. (1996). Two opsins from the compound eye of the crab Hemigrapsus sanguineus. Journal of Experimental Biology 199, 441–450.Google Scholar
Schloss, P.D. & Handelsman, J. (2005). Introducing Dotur, a computer program for defining operational taxonomic units and estimating species richness. Applied and Environmental Microbiology 71, 1501–1506.Google Scholar
Shi, W., Osawa, S., Dickerson, C.D. & Weiss, E.R. (1995). Rhodopsin mutants discriminate sites important for the activation of rhodopsin kinase and G (t). The Journal of Biological Chemistry 270, 2112.Google Scholar
Shi, J., Radlwimmer, F.B. & Yokoyama, S. (2001). Molecular genetics and the evoloution of ultraviolet vision in vertebrates. Proceedings of the National Academy of Science USA 98, 11731–11736.Google Scholar
Takahashi, Y. & Ebrey, T.G. (2003). Molecular basis of spectral tuning in the newt short wavelength sensitive visual pigment. Biochemistry 42, 6025–6034.Google Scholar
Terakita, A., Koyanagi, M., Tsukamoto, H., Yamashita, T., Miyata, T. & Shichida, Y. (2004). Counterion displacement in the molecular evolution of the rhodopsin family. Nature Structural and Molecular Biology 11, 284–289.Google Scholar
Terakita, A., Tsukamoto, H., Koyanagi, M., Sugahara, M., Yamashita, T. & Shichida, Y. (2008). Expression and comparative characterization of Gq-coupled invertebrate visual pigments and melanopsin. Journal of Neurochemistry 105, 883–890.Google Scholar
Wilkie, S.E., Robinson, P.R., Cronin, T.W., Poopalasundaram, S., Bowmaker, J.K. & Hunt, D.M. (2000). Spectral tuning of avian violet-and ultraviolet-sensitive visual pigments. Biochemistry 39, 7895–7901.Google Scholar
Yang, K., Farrens, D.L., Hubbell, W.L. & Khorana, H.G. (1996). Structure and function in rhodopsin: Single cysteine substitution mutants in the cytoplasmic interhelical E-F loop region show position-specific effects in transducin activation. Biochemistry 35, 12464–12469.Google Scholar
Yokoyama, S. (2000). Molecular evolution of vertebrate visual pigments. Progress in Retinal and Eye Research 19, 385–419.Google Scholar
Zylstra, P., Rothenfluh, H.S., Weiller, G.F., Blanden, R.V. & Steele, E.J. (1998). PCR amplification of murine immunoglobulin germline V genes: Strategies for minimization of recombination artifacts. Immunology and Cell Biology 76, 395–405.Google Scholar