全部 标题 作者
关键词 摘要

OALib Journal期刊
ISSN: 2333-9721
费用:99美元

查看量下载量

相关文章

更多...
PLOS ONE  2014 

Lake and Sea Populations of Mysis relicta (Crustacea, Mysida) with Different Visual-Pigment Absorbance Spectra Use the Same A1 Chromophore

DOI: 10.1371/journal.pone.0088107

Full-Text   Cite this paper   Add to My Lib

Abstract:

Glacial-relict species of the genus Mysis (opossum shrimps) inhabiting both fresh-water lakes and brackish sea waters in northern Europe show a consistent lake/sea dichotomy in eye spectral sensitivity. The absorbance peak (λmax) recorded by microspectrophotometry in isolated rhabdoms is invariably 20–30 nm red-shifted in “lake” compared with “sea” populations. The dichotomy holds across species, major opsin lineages and light environments. Chromophore exchange from A1 to A2 (retinal → 3,4-didehydroretinal) is a well-known mechanism for red-shifting visual pigments depending on environmental conditions or stages of life history, present not only in fishes and amphibians, but in some crustaceans as well. We tested the hypothesis that the lake/sea dichotomy in Mysis is due to the use of different chromophores, focussing on two populations of M. relicta from, respectively, a Finnish lake and the Baltic Sea. They are genetically very similar, having been separated for less than 10 kyr, and their rhabdoms show a typical lake/sea difference in λmax (554 nm vs. 529 nm). Gene sequencing has revealed no differences translating into amino acid substitutions in the transmembrane parts of their opsins. We determined the chromophore identity (A1 or A2) in the eyes of these two populations by HPLC, using as standards pure chromophores A1 and A2 as well as extracts from bovine (A1) and goldfish (A2) retinas. We found that the visual-pigment chromophore in both populations is A1 exclusively. Thus the spectral difference between these two populations of M. relicta is not due to the use of different chromophores. We argue that this conclusion is likely to hold for all populations of M. relicta as well as its European sibling species.

References

[1]  Audzijonyte A, Damgaard J, Varvio SL, Vainio JK, V?in?l? R (2005a) Phylogeny of Mysis (Crustacea, Mysida): history of continental invasions inferred from molecular and morphological data. Cladistics 21: 575–596. doi: 10.1111/j.1096-0031.2005.00081.x
[2]  V?in?l? R, Riddoch BJ, Ward RD, Jones RI (1994) Genetic zoogeography of the Mysis relicta species group (Crustacea: Mysidacea) in northern Europe and North America. Can J Fish Aquat Sci 51: 1490–1505. doi: 10.1139/f94-149
[3]  Lindstr?m M (2000) Eye function of Mysidacea (Crustacea) in the northern Baltic Sea. J Exp Mar Bio Ecol 246: 85–101. doi: 10.1016/s0022-0981(99)00178-1
[4]  Audzijonyte A, Pahlberg J, V?in?l? R, Lindstr?m M (2005b) Spectral sensitivity differences in two Mysis sibling species (Crustacea, Mysida): adaptation or phylogenetic constraints? J Exp Mar Bio Ecol 325: 228–239. doi: 10.1016/j.jembe.2005.05.007
[5]  Jokela-M??tt? M, Pahlberg J, Lindstr?m M, Zak P, Porter M, et al. (2005) Visual pigment absorbance and spectral sensitivity of Mysis relicta (Crustacea, Mysida) in different light environments. J Comp Physiol A 191: 1087–1097. doi: 10.1007/s00359-005-0039-8
[6]  Audzijonyte A, V?in?l? R (2006) Phylogeographic analyses of a circumarctic coastal and a boreal lacustrine mysid crustacean, and evidence of fast postglacial mtDNA rates. Mol Ecol 15: 3287–3301. doi: 10.1111/j.1365-294x.2006.02998.x
[7]  Audzijonyte A, Pahlberg J, Viljanen M, Donner K, V?in?l? R (2012) 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 21: 2176–2196. doi: 10.1111/j.1365-294x.2012.05516.x
[8]  Jokela-M??tt? M, Smura T, Aaltonen A, Ala-Laurila P, Donner K (2007) Visual pigments of Baltic Sea fishes of marine and limnic origin. Vis Neurosci 24: 389–398. doi: 10.1017/s0952523807070459
[9]  Nathans J (1990) Determinants of visual pigment absorbance: role of charged amino acids in the putative transmembrane segments. Biochemistry 29: 937–942. doi: 10.1021/bi00456a013
[10]  Asenjo AB, Rim J, Oprian DD (1994) Molecular determinants of human red/green color discrimination. Neuron 12: 1131–1138. doi: 10.1016/0896-6273(94)90320-4
[11]  Hunt DM, Dulai KS, Partridge JC, Cottrill P, Bowmaker JK (2001) The molecular basis of a spectral tuning of rod visual pigments in deep-sea fish. J Exp Biol 204: 3333–3344.
[12]  Hunt DM, Carvalho LS, Cowing JA, Davies WL (2009) Evolution and spectral tuning of visual pigments in birds and mammals. Philos Trans R Soc Lond B Biol Sci 364: 2941–2955. doi: 10.1098/rstb.2009.0044
[13]  Beatty DD (1974) Rhodopsin-porphyropsin changes in paired-pigment fishes. In: Vision in Fishes: New Approaches to Research (ed. M.A. Ali) 635–644. New York: Plenum Press.
[14]  Temple SE, Plate EM, Ramsden S, Haimberger TJ, Roth WM, et al. (2006) Seasonal cycle in vitamin A1/A2-based visual pigment composition during the life history of Coho Salmon (Oncorhynchus Kisutch). J Comp Physiol A 192: 301–313. doi: 10.1007/s00359-005-0068-3
[15]  Wald G (1946) The metamorphosis of visual system in Amphibia. Biol Bull 91: 239.
[16]  Reuter T (1969) Visual pigments and ganglion cell activity in the retinae of tadpoles and adult frogs (Rana temporaria L.). Acta Zool Fenn 122: 1–64.
[17]  Reuter TE, White RH, Wald G (1971) Rhodopsin and porphyropsin fields in the adult bullfrog retina. J Gen Physiol 58: 351–371. doi: 10.1085/jgp.58.4.351
[18]  Bowmaker JK, Dartnall HJA, Herring PJ (1988) Longwave-sensitive visual pigments in some deep-sea fishes: segregation of “paired” rhodopsins and porphyropsins. J Comp Physiol A 163: 685–698. doi: 10.1007/bf00603853
[19]  Saarinen P, Pahlberg J, Herczeg G, Viljanen M, Karjalainen M, et al. (2012) Spectral tuning by selective chromophore uptake in rods and cones of eight populations of nine-spined stickleback (Pungitius pungitius). J Exp Biol 215: 2760–2773. doi: 10.1242/jeb.068122
[20]  Dartnall HJ, Lythgoe JN (1965) The spectral clustering of visual pigments. Vision Research 5: 81–100. doi: 10.1016/0042-6989(65)90057-x
[21]  Hárosi FI (1994) An analysis of two spectral properties of vertebrate visual pigments. Vision Res 34: 1359–1367. doi: 10.1016/0042-6989(94)90134-1
[22]  Whitmore AV, Bowmaker JK (1989) Seasonal variation in cone sensitivity and short-wave absorbing visual pigments in the rudd Scardinius erythrophthalmus. J Comp Physiol A 166: 103–115. doi: 10.1007/bf00190215
[23]  Suzuki T, Makino-Tasaka M, Eguchi E (1984) 3-Dehydroretinal (vitamin A2 aldehyde) in crayfish eye. Vision Res 24: 783–787. doi: 10.1016/0042-6989(84)90149-4
[24]  Suzuki T, Eguchi E (1987) A survey of 3-dehydroretinal as a visual pigment chromophore in various species of crayfish and other freshwater crustaceans. Experientia 43: 1111–1113. doi: 10.1007/bf01956053
[25]  Suzuki T, Arigawa K, Eguchi E (1985) The effects of light and temperature on the rhodopsin-porphyropsin visual system of the crayfish Procambarus clarkii. Zoolog Sci 2: 455–461.
[26]  Eronen M, Glückert G, Hatakka L, van de Plassche O, van der Plicht J, et al. (2001) Rates of Holocene isostatic uplift and relative sea-level lowering of the Baltic in SW Finland based on studies of isolation contacts. Boreas 30: 17–30. doi: 10.1080/030094801300062248
[27]  Ala-Laurila P, Pahlberg J, Koskelainen A, Donner K (2004) On the relation between the photoactivation energy and the absorbance spectrum of visual pigments. Vision Res 44: 2153–2158. doi: 10.1016/j.visres.2004.03.031
[28]  Ala-Laurila P, Donner K, Koskelainen A (2004) Thermal activation and photoactivation of visual pigments. Biophys J 86: 3653–3662. doi: 10.1529/biophysj.103.035626
[29]  Pahlberg J, Lindstr?m M, Ala-Laurila P, Fyhrquist-Vanni N, Koskelainen A, et al. (2005) The photoactivation energy of the visual pigment in two spectrally different populations of Mysis relicta (Crustacea, Mysida). J Comp Physiol A 191: 837–844. doi: 10.1007/s00359-005-0005-5
[30]  von Planta C, Schweiter U, Chopard-dit JL, Ruegg R, Kofler M, et al. (1962) Synthesen in der Vitamin A2-Reihe. 4. Physikalische Eigenschaften von Isomeren Vitamin A und Vitamin A2 Verbindungen. Helv Chim Acta 45: 548–561. doi: 10.1002/hlca.19620450218
[31]  Liu RSH, Asato AE (1984) Photochemistry and synthesis of stereoisomers of vitamin A. Tetrahedron. 40: 1931–1969. doi: 10.1016/s0040-4020(01)88435-0
[32]  Williams TP, Milby SE (1968) The thermal decomposition of some visual pigments. Vision Res 8: 359–367. doi: 10.1016/0042-6989(68)90105-3
[33]  Papermaster DS (1982) Preparation of rod outer segments. Methods Enzymol 81: 48–52. doi: 10.1016/s0076-6879(82)81010-0
[34]  Fomin MA, Belikov NE, Lukin AYu, Laptev AV, Demina OV et al. Patent RU No 2417983. The preparation of 11-cis-isomer of retinal.//cl. C07C403/14; priority 30.10.2009, appl. No 2009140175 from 30.10.2009. Published 10.05.2011: Bulletin Izobreteniya. Poleznye modeli No 13. MPC C07C 403/14: P.13 (in Russian)..
[35]  Murakami M, Kouyama T (2008) Crystal structure of squid rhodopsin. Nature 453: 363–368. doi: 10.1038/nature06925
[36]  Woltereck R (1909) Weitere experimentelle Untersuchungen über Artver?nderung, speziell über das Wesen quantitativer Artunterschiede bei Daphniden. Verhandlungen der deutschen zoologischen Gesellschaft 19: 110–73. doi: 10.1007/bf01876686
[37]  Shand J (1993) Changes in the spectral absorption of cone visual pigments during the settlement of the goatfish Upeneus tragula: the loss of red sensitivity as a benthic existence begins. J Comp Physiol A 173: 115–121. doi: 10.1007/bf00209623
[38]  Browman HI, Hawryshyn CW (1994) The developmental trajectory of ultraviolet photosensitivity in rainbow trout is altered by thyroxine. Vision Res 34: 1397–1406. doi: 10.1016/0042-6989(94)90139-2
[39]  Archer S, Hope A, Partridge JC (1995) The molecular basis for the green-blue sensitivity shift in the rod visual pigments of the European eel. Proc R Soc Lond B Biol Sci 262: 289–295. doi: 10.1098/rspb.1995.0208
[40]  Hope AJ, Partridge JC, Hayes PK (1998) Switch in rod opsin gene expression in the European eel, Anguilla anguilla (L.). Proc R Soc Lond B Biol Sci 265: 869–874. doi: 10.1098/rspb.1998.0372
[41]  Carleton KL, Kocher TD (2001) Cone opsin genes of African cichlid fishes: tuning spectral sensitivity by differential gene expression. Mol Biol Evol 18: 1540–1550. doi: 10.1093/oxfordjournals.molbev.a003940
[42]  Shand J, Hart NS, Thomas N, Partridge JC (2002) Developmental changes in the cone visual pigments of black bream Acanthopagnus butcheri. J Exp Biol 205: 3661–3667.
[43]  Parry JW, Carleton KL, Spady T, Carboo A, Hunt DM, et al. (2005) Mix and match color vision: tuning spectral sensitivity by differential opsin gene expression in Lake Malawi cichlids. Curr Biol 15: 1734–1739. doi: 10.1016/j.cub.2005.08.010
[44]  Spady TC, Parry JW, Robinson PR, Hunt DM, Bowmaker JK, et al. (2006) Evolution of the cichlid visual palette through ontogenetic subfunctionalization of the opsin gene array. Mol Biol Evol 23: 1538–1547. doi: 10.1093/molbev/msl014
[45]  Zak P, Lindstr?m M, Demchuk JuV, Donner K, Ostrovsky MA (2013) The eye of the opossum shrimp Mysis relicta (Crustacea, Mysidae) contains two visual pigments located in different photoreceptor cells. Dokl Biol Sci 449: 68–72. doi: 10.1134/s0012496613020026
[46]  Lindstr?m M, Nilsson HL (1988) Eye function of Mysis relicta Lovén (Crustacea) from two photic environments. Spectral sensitivity and light tolerance. J Exp Mar Bio Ecol 120: 23–37. doi: 10.1016/0022-0981(88)90216-x
[47]  Gal G, Loew ER, Rudstam LG, Mohammadian AM (1999) Light and diel vertical migration: Spectral sensitivity and light avoidance by Mysis relicta. Can J Fish Aquat Sci 56: 311–322. doi: 10.1139/cjfas-56-2-311
[48]  Boscarino BT, Rudstam LG, Loew ER, Mills EL (2009) Predicting the vertical distribution of the opossum shrimp, Mysis relicta, in Lake Ontario: a test of laboratory-based light preferences. Can J Fish Aquat Sci 66: 101–113. doi: 10.1139/f08-190
[49]  Donner K, Firsov ML, Govardovskii VI (1990) The frequency of isomerization-like ‘dark’ events in rhodopsin and porphyropsin rods of the bull-frog retina. J Physiol 428: 673–692.
[50]  Ala-Laurila P, Donner K, Crouch RK, Cornwall MC (2007) Chromophore switch from 11-cis-dehydroretinal (A2) to 11-cis-retinal (A1) decreases dark noise in salamander red rods. J Physiol 585: 57–74. doi: 10.1113/jphysiol.2007.142935
[51]  Govardovskii VI, Fyhrquist N, Reuter T, Kuzmin DG, Donner K (2000) In search of the visual pigment template. Vis Neurosci 17: 509–528. doi: 10.1017/s0952523800174036

Full-Text

Contact Us

service@oalib.com

QQ:3279437679

WhatsApp +8615387084133