Skip to main content
SpringerLink
Log in

Rhodopsin: Evolution and comparative physiology

  • Published:
Paleontological Journal Aims and scope Submit manuscript

Abstract

A review of physicochemical properties, photochemistry, functions, and evolution of retinal-containing proteins (microbial and of metazoan rhodopsins, mostly visual rhodopsins) is provided. Comparative physiology of visual rhodopsins is considered in detail, mainly the molecular mechanisms of their spectral tuning.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Abu-Khamidakh, E., Demchuk, Yu.V., Zak, P.P., et al., Shortwave light filtration in the formation of spectral sensitivity in two populations of the shrimp M. relicta (Mysida), Vestn. Mosk. Gos. Univ. Ser. Biol., 2010, no. 2, pp. 9–14.

    Google Scholar 

  • Audzijonyte, A., Pahlberg, J., Viljanen, M., et al., Opsin gene sequence variation across phylogenetic and population histories in Mysis (Crustacea: Mysida) does not match current light environments or visual-pigment absorbance spectra, Mol. Ecol., 2012, vol. 21, pp. 2176–2196.

    Article  Google Scholar 

  • Belikov, N., Yakovleva, M., Feldman, T., et al., Lake and sea populations of Mysis relicta (Crustacea, Mysida) with different visual-pigment absorbance spectra use the same A1 chromophore, PLoS, 2014, vol. 9, no. 2, pp. 1–8.

    Google Scholar 

  • Bowmaker, J.K. and Hunt, D.M., Evolution of vertebrate visual pigments, Curr. Biol., 2006, vol. 16, no. 13, pp. 484–489.

    Article  Google Scholar 

  • Bridges, C.D.B., The rhodopsin–porphyropsin visual system, in Handbook of Sensory Physiology, vol. 2. Photochemistry of Vision, Dartnall, H.J.A., Ed., Berlin: Springer, 1972, pp. 417–480.

    Google Scholar 

  • Collin, S.P., Knight, M.A., Davies, W.L., et al., Ancient colour vision: Multiple opsin genes in the ancestral vertebrates, Curr. Biol., 2003, vol. 13, pp. 864–865.

    Article  Google Scholar 

  • Consani, C., Braem, O., and Oskouei, A.A., Ultrafast (bio)physical and (bio)chemical dynamics, Chimia (Aarau.), 2011, vol. 65, no. 9, pp. 683–690.

    Article  Google Scholar 

  • Dartnall, H.A.J. and Lythgoe, J.N., The spectral clustering of visual pigments, Vis. Res., 1965, vol. 5, pp. 81–100.

    Article  Google Scholar 

  • Darwin, C., On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life, London: John Murray, 1859.

    Book  Google Scholar 

  • Deisseroth, K., Optogenetics: 10 years of microbial opsins in neuroscience, Nature Neurosci., 2015, vol. 18, no. 9, pp. 1213–1225.

    Article  Google Scholar 

  • Dolgikh, D.A., Malyshev, A.Yu., Salozhin, S.V., et al., Anion channel rhodopsin, expressed in culture of neurons and in vivo in the mouse brain: Light-induced suppression of generation of potentials of action, Dokl. Akad. Nauk, 2015, vol. 465, no. 6, pp. 737–740.

    Google Scholar 

  • Donner, K., Zak, P., Viljanen, M., et al., Eye special sensitivity in fresh- and brackish populations of three glacial-relict Mysis species (Crustacea): Physiology and genetics of differential tuning, J. Comp. Physiol. Ser. A, 2016, vol. 202, no. 4, pp. 297–312.

    Article  Google Scholar 

  • Dontsov, A.E., Fedorovich, I.B., Lindstrom, M., and Ostrovsky, M.A., Comparative study of spectral and antioxidant properties of pigments from the eyes of two Mysis relicta (Crustacea, Mysidacea) populations, with different light damage resistance, J. Comp. Physiol. Ser. B, 1999, vol. 169, no. 3, pp. 157–164.

    Article  Google Scholar 

  • Enright, J.M., Toomey, M.B., Sato, S., et al., Cyp27c1 redshifts the spectral sensitivity of photoreceptors by converting vitamin A1 into A2, Curr. Biol., 2015, vol. 25, pp. 3048–3057.

    Article  Google Scholar 

  • Feldman, T.B., Femtosecond spectroscopic study of photochromic reactions of bacterial and animal rhodopsins, Photochem. Photobiol. (in press).

  • Feldman, T., Yakovleva, M., Lindström, M., et al., Eye adaptation to different light environment in two populations of Mysis relicta: A comparative study of carotenoids and retinoids, J. Crustac. Biol., 2010, vol. 30, no. 4, pp. 636–642.

    Article  Google Scholar 

  • Feuda, R., Hamilton, S.C., McInerney, J.O., and Pisani, D., Metazoan opsin evolution reveals a simple route to animal vision, Proc. Nat. Acad. Sci. USA, 2012, vol. 109, pp. 18868–18872.

    Article  Google Scholar 

  • Fitch, M., Distinguishing homologous from analogous proteins, Syst. Zool., 1970, vol. 19, no. 2, pp. 99–113.

    Article  Google Scholar 

  • Frank, T.M., Porter, M., and Cronin, T.W., Spectral sensitivity, visual pigments and screening pigments in two life history stages of the ontogenetic migrator Gnathophausia ingens, J. Mar. Biol. Assoc. UK, 2009, vol. 89, no. 1, pp. 119–129.

    Article  Google Scholar 

  • Fuhrman, J.A., Schwalbach, M.S., and Stingl, U., Proteorhodopsins: An array of physiological roles?, Nature Rev. Microbiol., 2008, vol. 6, no. 6, pp. 488–494.

    Google Scholar 

  • Gelis, L., Wolf, S., Hatt, H., et al., Prediction of a ligandbinding niche within a human olfactory receptor by combining site-directed mutagenesis with dynamic homology modeling, Angew. Chem., Int. Ed. Engl., 2012, vol. 51, pp. 1274–1278.

    Article  Google Scholar 

  • Govardovsky, L.A. and Astakhov, M.L., Specificit of physiological and biochemical mechanisms of excitation and adaptation of cones in the retina, Sensor. Sist., 2015, vol. 29, no. 4, pp. 296–308.

    Google Scholar 

  • Govorunova, E.G., Sineshchekov, O.A., Janz, R., et al., Natural light-gated anion channels: A family of microbial rhodopsins for advanced optogenetics, Science, 2015, vol. 349, no. 6248, pp. 647–650.

    Article  Google Scholar 

  • Grote, M. and O’Malley, M.A., Enlightening the life sciences: The history of halobacterial and microbial rhodopsin research, FEMS Microbiol. Rev., 2011, vol. 35, no. 6, pp. 1082–1099.

    Article  Google Scholar 

  • Hankins, M., Peirson, S., and Foster, R., Melanopsin: An exciting photopigment, Trends Neurosci., 2008, vol. 3, pp. 27–36.

    Article  Google Scholar 

  • Harosi, F.I., An analysis of two spectral properties of vertebrate visual pigments, Vis. Res., 1994, vol. 34, pp. 1359–1367.

    Article  Google Scholar 

  • Hunt, D.M., Carvalho, L.S., Cowing, J.A., et al., Spectral tuning of shortwave-sensitive visual pigments in vertebrates, Photochem. Photobiol., 2007, vol. 83, no. 2, pp. 303–310.

    Article  Google Scholar 

  • Jokela-Maatta, M., Pahlberg, J., Lindstrom, M., et al., Visual pigment absorbance and spectral sensitivity of the Mysis relicta species group (Crustacea, Mysida) in different light environments, J. Comp. Physiol. A, 2005, vol. 191, no. 12, pp. 1087–1097.

    Article  Google Scholar 

  • Katritch, V., Cherezov, V., and Stevens, R.C., Diversity and modularity of G protein-coupled receptor structures, Trends Pharm. Sci., 2012, vol. 33, no. 1, pp. 17–27.

    Article  Google Scholar 

  • Khain, V.E., On the mainstreams in modern Earth sciences, Vestn. Mosk. Ross. Akad. Nauk. 2009, vol. 79, no. 1, pp. 50–56.

    Google Scholar 

  • Kirpichnikov, M.P. and Ostrovsky, M.A., and prosthetics of degenerative retina, Vestn. Oftal’m., 2015, vol. 131, no. 3, pp. 99–111.

    Article  Google Scholar 

  • Krishnan, A., Almen, M.S., Fredriksson, R., and Schioth, H.B., The origin of GPCRs: Identification of mammalian like rhodopsin, adhesion, glutamate and frizzled GPCRs in fungi, PLoS, 2012, vol. 7, pp. e29817.

    Article  Google Scholar 

  • Lamb, T.D., Evolution of vertebrate retinal photoreception, Phil. Trans. Roy. Soc. B, 2009, vol. 364, no. 1531, pp. 2911–2924.

    Article  Google Scholar 

  • Lamb, T.D., Evolution of the eye: Scientists now have a clear vision of how our notoriously complex eye came to be, Sci. Am., 2011, vol. 305, no. 1, pp. 64–69.

    Article  Google Scholar 

  • Lamb, T.D., Collin, S.P., and Pugh, E.N., Jr., Evolution of the vertebrate eye: Opsins, photoreceptors, retina and eye cup, Nature Rev. Neurosci., 2007, vol. 8, pp. 960–975.

    Article  Google Scholar 

  • Li, J., Edwards, P.C., Burghammer, M., et al., Structure of bovine rhodopsin in a trigonal crystal form, J. Mol. Biol., 2004, vol. 343, pp. 1409–1413.

    Article  Google Scholar 

  • Lindstrom, M., Eye function of Mysidacea (Crustacea) in the northern Baltic Sea, J. Exp. Mar. Biol. Ecol., 2000, vol. 246, pp. 85–101.

    Article  Google Scholar 

  • Lindstrom, M. and Nilsson, H.L., Eye function of Mysis relicta (Crustacea) from two photic environments: Spectral sensitivity and light tolerance, J. Exp. Mar. Biol. Ecol., 1988, vol. 120, pp. 23–37.

    Article  Google Scholar 

  • Luk, H.L., Melaccio, F., Rinaldi, S., et al., Molecular bases for the selection of the chromophore of animal rhodopsins, Proc. Nat. Acad. Sci. USA, 2015, vol. 112, pp. 15297–15302.

    Article  Google Scholar 

  • Mackin, A., Roy, R.A., and Theobald, D.L., An empirical test of convergent evolution in rhodopsins, Mol. Biol. Evol., 2014, vol. 31, pp. 85–95.

    Article  Google Scholar 

  • Mancuso, K., Hauswirth, W.W., and Li, Q., Gene therapy for redgreen colour blindness in adult primates, Nature, 2009, vol. 461, pp. 784–787.

    Article  Google Scholar 

  • Martinez, T.J., Seaming is believing, Nature, 2010, vol. 467, pp. 412–413.

    Article  Google Scholar 

  • Nadtochenko, V.A., Smitienko, O.A., Feldman, T.B., et al., Conical intersection participation in femtosecond dynamics of visual pigment rhodopsin chromophore cis-trans photoisomerization, Dokl. Biochem. Biophys., 2012, vol. 446, pp. 242–246.

    Article  Google Scholar 

  • Nilson, D.E., Eye evolution and its functional basis, Vis. Neurosci., 2013, vol. 30, pp. 5–20.

    Article  Google Scholar 

  • Nilsson, H.L., Eye function of Mysis relicta (Crustacea) from two photic environments: Spectral sensitivity and light tolerance, J. Exp. Mar. Biol. Ecol., 1988, vol. 120, pp. 23–37.

    Article  Google Scholar 

  • Nordstreom, K.J., Almren, M.S., Edstam, M.M., et al., Independent HH search, Needleman–Wunsch-based, and motif analyses reveal the overall hierarchy for most of the G protein-coupled receptor families, Mol. Biol. Evol., 2011, vol. 28, no. 9, pp. 2471–2480.

    Article  Google Scholar 

  • Novitsky, I.Yu., Zak, P.P., and Ostrovsky, M.A., Influence of anions on spectral properties of iodopsin in native cones of the retina of frog (microspectrophotometric investigation), Bioorgan. Khimiya., 1989, vol. 15, no. 8, pp. 1037–1043.

    Google Scholar 

  • Ostrovsky, M.A., Chapter 5. Photoreception, in Rukovodstvo po fiziologii (Handbook on Physiology), vol. 5. Fiziologiya sensornykh sistem. Chast’ 1. Fiziologiya zreniya (Physiology of Sensory Systems: Part 1. Physiology of Vision), Leningrad: Nauka, 1971, pp. 88–119.

    Google Scholar 

  • Ostrovsky, M.A. and Feldman, T.B., Chemistry and molecular physiology of vision: Photosensitive protein rhodopsin, Usp. Khim., 2012, vol. 81, no. 11, pp. 1071–1090.

    Article  Google Scholar 

  • Ostrovsky, M.A. and Kirpichnikov, M.P., Optogenetics and vision, Sens. Sist., 2015, vol. 25, no. 4, pp. 289–295.

    Google Scholar 

  • Park, J.H., Morizumi, T., Li, Y., et al., Opsin, a structural model for olfactory receptors?, Angew. Chem., Int. Ed. Engl., 2013, vol. 52, pp. 11021–11024.

    Article  Google Scholar 

  • Pele, J., Abdi, H., Moreau, M., et al., Multidimensional scaling reveals the main evolutionary pathways of class A Gprotein-coupled receptors, PLoS, 2011, vol. 6, pp. e19094.

    Article  Google Scholar 

  • Pierce, K.L., Premont, R.T., and Lefkowitz, R.J., Signalling: Seven-transmembrane receptors, Nat. Rev. Mol. Cell Biol., 2002, vol. 3, pp. 639–650.

    Article  Google Scholar 

  • Polli, D., Altoè, P., and Weingart, O., Conical intersection dynamics of the primary photoisomerization event in vision, Nature, 2010, vol. 467, pp. 440–443.

    Article  Google Scholar 

  • Rodieck, R.W., The First Steps in Seeing, Sunderland: Sinauer Assoc., 1998.

    Google Scholar 

  • Rozanov, A.Yu., Life conditions on the early Earth after 4.0 Ga, in Problemy proiskhozhdeniya zhizni (Problems of the Origin of Life), Moscow: Paleontol. Inst. Ross. Akad. Nauk, 2009, pp. 185–201.

    Google Scholar 

  • Schoenlein, R.W., Peteanu, L.A., Mathies, R.A., and Shank, C.V., The first step in vision: Femtosecond isomerization of rhodopsin, Science, 1991, vol. 254, pp. 412–415.

    Article  Google Scholar 

  • Schwanzara, S.A., The visual pigments of freshwater fishes, Vis. Res., 1967, vol. 7, pp. 121–148.

    Article  Google Scholar 

  • Shen, L., Chen, C., Zheng, H., and Jin, L., The evolutionary relationship between microbial rhodopsins and Metazoan rhodopsins, Sci. World J., 2013. http://dx.doi.org/. doi 0.1155/2013/435651

    Google Scholar 

  • Sineshchekov, O.A., Jung, KH., and Spudich, J.L., Two rhododopsins mediate phototaxis to low- and high-intensity light in Chlamydomonas reinhardtii, Proc. Nat. Acad. Sci. USA, 2002, vol. 99, no. 13, pp. 8689–8694.

    Article  Google Scholar 

  • Slobodyanskaya, E.M., Abrashin, E.V., and Ostrovsky, M.A., Investigation of ionochromic properties of visual pigments in chicken, Bioorgan. Khim., 1980, vol. 6, no. 2, pp. 223–229.

    Google Scholar 

  • Smitienko, O., Nadtochenko, V., Feldman, T., et al., Femtosecond laser spectroscopy of the rhodopsin photochromic reaction: A concept for ultrafast optical molecular switch creation, Molecules, 2014, vol. 19, no. 11, pp. 18351–18366.

    Article  Google Scholar 

  • Spudich, J.L., Yang, C.S., Jung, K.H., and Spudich, E.N., Retinylidene proteins: Structures and functions from archaea to humans, Ann. Rev. Cell. Dev. Biol., 2000, vol. 16, pp. 365–392.

    Article  Google Scholar 

  • Suzuki, T., Arigawa, K., and Eguchi, E., The effects of light and temperature on the rhodopsin-porphyropsin visual system of the crayfish Procambarus clarkia, Zool. Sci., 1985, vol. 2, pp. 455–461.

    Google Scholar 

  • Suzuki, T., Makino-Tasaka, M., and Eguchi, E., 3-dehydroretinal (vitamin A2 aldehyde) in crayfish eye, Vis. Res., 1984, vol. 24, no. 8, pp. 783–787.

    Article  Google Scholar 

  • Suzuki, T., Terakita, A., and Tsin, A.T.C., Retinoid metabolism and conversion of retinol to dehydroretinol in the crayfish (Procambarus clarkii) retina, Comp. Biochem. Physiol., 1993, vol. 105B, pp. 257–261.

    Google Scholar 

  • Temple, S.E., Plate, E.M., Ramsden, S., et al., Seasonal cycle in vitamin A1/A2-based visual pigment composition during the life history of coho salmon (Oncorhynchus kisutch), J. Comp. Physiol. A, 2006, vol. 192, pp. 301–313.

    Article  Google Scholar 

  • Terakita, A., The opsins, Genome Biol., 2005, vol. 6, no. 3, pp. 213.1–213.9.

    Article  Google Scholar 

  • Walls, G.L., The Vertebrate Eye and Its Adaptive Radiation, Bloomfield Hills: Cranbrook Inst. of Sci., 1942.

    Book  Google Scholar 

  • Wand, A., Gdor, I., Zhu, J., et al., Shedding new light on retinal protein photochemistry, Ann. Rev. Phys. Chem., 2013, vol. 64, pp. 437–458.

    Article  Google Scholar 

  • Waschuk, S.A., Bezerra, A.G., Shi, L., and Brown, L.S., Leptosphaeria rhodopsin: Bacteriorhodopsin-like proton pump from an eukaryote, Proc. Nat. Acad. Sci. USA, 2005, vol. 102, no. 19, pp. 6879–6883.

    Article  Google Scholar 

  • Wolf, S. and Grunewald, S., Sequence, structure and ligand binding evolution of rhodopsin-like G protein-coupled receptors: A crystal structure-based phylogenetic analysis, PLoS, 2015, vol. 10, no. 4, pp. e0123533.

    Article  Google Scholar 

  • Zak, P.P., Lindströ m, M., Demchuk, Yu.V., et al., Eyes of the shrimp Mysis relicta (Crustacea, Mysidae) contain two types of visual pigments located in different photoreceptors, Dokl. Ross. Akad. Nauk, 2013, vol. 449, no. 2, pp. 240–245.

    Google Scholar 

  • Zak, P.P., Ostrovsky, M.A., and Bowmaker, J.K., Ionochronic properties of long-wave-sensitive cones in the goldfish retina: An electrophysiological and microspectrophotometric study, Vis. Res., 2001, vol. 41, pp. 1755–1763.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Emanuel Institute of Biochemical Physics, Russian Academy of Sciences, ul. Kosygina 4, Moscow, 117977, Russia

    M. A. Ostrovsky

Authors
  1. M. A. Ostrovsky
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. A. Ostrovsky.

Additional information

Original Russian Text © M.A. Ostrovsky, 2017, published in Paleontologicheskii Zhurnal, 2017, No. 5, pp. 103–113.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ostrovsky, M.A. Rhodopsin: Evolution and comparative physiology. Paleontol. J. 51, 562–572 (2017). https://doi.org/10.1134/S0031030117050069

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0031030117050069

Keywords

Search

Navigation