Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-15T13:21:17.818Z Has data issue: false hasContentIssue false
  • English
  • Français

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: [email protected]
Get access Rights & Permissions [Opens in a new window]

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

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abascal, F., Zardoya, R. & Posada, D. (2005). ProtTest: Selection of best-fit models of protein evolution. Bioinformatics 21, 2104–2105.CrossRefGoogle ScholarPubMed
Ahyong, S.T. & Harling, C. (2000). The phylogeny of the stomatopod Crustacea. Australian Journal of Zoology 48, 607–642.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle 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), 47–54.3.0.CO;2-F>CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Bowmaker, J.K. & Hunt, D.M. (2006). Evolution of vertebrate visual pigments. Current Biology 16, R484–R489.CrossRefGoogle ScholarPubMed
Bradley, R.D. & Hillis, D.M. (1997). Recombinant DNA sequences generated by PCR amplification. Molecular Biology and Evolution 14, 592–593.CrossRefGoogle ScholarPubMed
Briscoe, A.D. (2001). Functional diversification of lepidopteran opsins following gene duplication. Molecular Biology and Evolution 18, 2270–2279.CrossRefGoogle ScholarPubMed
Briscoe, A.D. & Chittka, L. (2001). The evolution of color vision in insects. Annual Review of Entomology 46, 471–510.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle 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.CrossRefGoogle Scholar
Contreras-Moreira, B. & Bates, P.A. (2002). Domain fishing: A first step in protein comparative modelling. Bioinformatics 18, 1141–1142.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Cronin, T.W. (1985). The visual pigment of a stomatopod crustacean, Squilla empusa. Journal of Comparative Physiology A 156, 679–687.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Do, C.B., Mahabhashyam, M.S.P, Brudno, M. & Batzoglou, S. (2005). Probcons: Probabilistic consistency-based multiple sequence alignment. Genome Research 15, 330–340.CrossRefGoogle ScholarPubMed
Fasick, J.I., Applebury, M.L. & Oprian, D.D. (2002). Spectral tuning in the mammalian shortwavelength sensitive cone pigments. Biochemistry 41, 6860–6865.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Guex, N. & Peitsch, M.C. (1997). Swiss-model and the Swiss-Pdb Viewer: An environment for comparative protein modeling. Electrophoresis 18, 2714–2723.CrossRefGoogle Scholar
Guindon, S. & Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696–704.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Huber, T., Faulkner, G. & Hugenholtz, P. (2004). Bellerophon: A program to detect chimeric sequences in multiple sequence alignments. Bioinformatics 20, 2317–2319.CrossRefGoogle ScholarPubMed
Janz, J.M. & Farrens, D.L. (2001). Engineering a functional blue-wavelength-shifted rhodopsin mutant. Biochemistry 40, 7219–7227.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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 ScholarPubMed
Murakami, M. & Kouyama, T. (2008). Crystal structure of squid rhodopsin. Nature 453, 363–367.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Nathans, J. (1990). Determinants of visual pigment absorbance: identification of the retinyidene Schiff's base counterion in bovine rhodopsin. Biochemistry 29, 9746–9752.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Takahashi, Y. & Ebrey, T.G. (2003). Molecular basis of spectral tuning in the newt short wavelength sensitive visual pigment. Biochemistry 42, 6025–6034.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Yokoyama, S. (2000). Molecular evolution of vertebrate visual pigments. Progress in Retinal and Eye Research 19, 385–419.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar