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Deep-sea and pelagic rod visual pigments identified in the mysticete whales

Published online by Cambridge University Press:  09 March 2012

NICOLE BISCHOFF ,
BENJAMIN NICKLE ,
THOMAS W. CRONIN ,
STEPHANI VELASQUEZ  and
JEFFRY I. FASICK
NICOLE BISCHOFF
Affiliation:
The New Jersey Center for Science, Technology & Mathematics, Kean University, Union, New Jersey
BENJAMIN NICKLE
Affiliation:
Department of Biochemistry, Brandeis University, Waltham, Massachusetts
THOMAS W. CRONIN
Affiliation:
Department of Biological Sciences, University of Maryland, Baltimore, Maryland
STEPHANI VELASQUEZ
Affiliation:
Graduate School of Biomedical Sciences, University of Medicine and Dentistry of New Jersey, Newark, New Jersey
JEFFRY I. FASICK*
Affiliation:
School of Environmental and Life Sciences, Kean University, Union, New Jersey
*
*Address correspondence and reprint requests to: Jeffry I. Fasick, School of Environmental and Life Sciences, Kean University, 1000 Morris Avenue, Union, NJ 07083. E-mail: [email protected]
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Abstract

Our current understanding of the spectral sensitivities of the mysticete whale rod-based visual pigments is based on two species, the gray whale (Eschrichtius robustus) and the humpback whale (Megaptera novaeangliae) possessing absorbance maxima determined from difference spectra to be 492 and 497 nm, respectively. These absorbance maxima values are blueshifted relative to those from typical terrestrial mammals (≈500 nm) but are redshifted when compared to those identified in the odontocetes (479–484 nm). Although these mysticete species represent two of the four mysticete families, they do not fully represent the mysticete whales in terms of foraging strategy and underwater photic environments where foraging occurs. In order to better understand the spectral sensitivities of the mysticete whale rod visual pigments, we have examined the rod opsin genes from 11 mysticete species and their associated amino acid substitutions. Based on the amino acids occurring at positions 83, 292, and 299 along with the directly determined dark spectra from expressed odontocete and mysticete rod visual pigments, we have determined that the majority of mysticete whales possess deep-sea and pelagic like rod visual pigments with absorbance maxima between 479 and 484 nm. Finally, we have defined the five amino acid substitution events that determine the resulting absorbance spectra and associated absorbance maxima for the mysticete whale rod visual pigments examined here.

Keywords

BaleenCetaceanOpsinAbsorbance spectraAmino acid substitution
Type
Research Articles
Information
Visual Neuroscience , Volume 29 , Issue 2 , March 2012 , pp. 95 - 103
Copyright
Copyright © Cambridge University Press 2012

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References

Baumgartner, M.F. & Mate, B.R. (2003). Summertime foraging ecology of North Atlantic right whales. Marine Ecology Progress Series 264, 123–135.CrossRefGoogle Scholar
Chan, T., Lee, M. & Sakmar, T.P. (1992). Introduction of hydroxyl-bearing amino acids causes bathochromic spectral shifts in rhodopsin. Amino acid substitutions responsible for red-green color pigment spectral tuning. The Journal of Biological Chemistry 267, 9478–9480.CrossRefGoogle ScholarPubMed
Chang, B.S., Crandall, K.A., Carulli, J.P. & Hartl, D.L. (1995). Opsin phylogeny and evolution: A model for blue shifts in wavelength regulation. Molecular Phylogenetics and Evolution 4, 31–43.CrossRefGoogle Scholar
Davies, J.L. & Guiler, E.R. (1957). A note on the pygmy right whale, Caperea marginata gray. Proceedings of the Zoological Society of London 129, 579–589.CrossRefGoogle Scholar
Fasick, J.I., Bischoff, N., Brennan, S., Velasquez, S. & Andrade, G. (2011). Estimated absorbance spectra of the visual pigments of the North Atlantic right whale (Eubalaena glacialis). Marine Mammal Science 27, E321–E331.CrossRefGoogle Scholar
Fasick, J.I., Cronin, T.W., Hunt, D.M. & Robinson, P.R. (1998). The visual pigments of the bottlenose dolphin (Tursiops truncatus). Visual Neuroscience 15, 643–651.CrossRefGoogle ScholarPubMed
Fasick, J.I. & Robinson, P.R. (1998). Mechanism of spectral tuning in the dolphin visual pigments. Biochemistry 37, 433–438.CrossRefGoogle ScholarPubMed
Fasick, J.I. & Robinson, P.R. (2000). Spectral-tuning mechanisms of marine mammal rhodopsins and correlations with foraging depth. Visual Neuroscience 17, 781–788.CrossRefGoogle ScholarPubMed
Franke, R.R., Sakmar, T.P., Oprian, D.D. & Khorana, H.G. (1988). A single amino acid substitution in rhodopsin (lysine 248→leucine) prevents activation of transducin. The Journal of Biological Chemistry 263, 2119–2122.CrossRefGoogle ScholarPubMed
Goldbogen, J.A., Calambokidis, J., Croll, D.A., Harvey, J.T., Newton, K.M., Oleson, E.M., Schorr, G. & Shadwick, R.E. (2008). Foraging behavior of humpback whales: Kinematic and respiratory patterns suggest a high cost for a lunge. The Journal of Experimental Biology 211, 3712–3719.CrossRefGoogle ScholarPubMed
Goldbogen, J.A., Calambokidis, J., Oleson, E.M., Potvin, J., Pyenson, N.D., Schorr, G. & Shadwick, R.E. (2011). Mechanics, hydrodynamics and energetics of blue whale lunge feeding: Efficiency dependence on krill density. The Journal of Experimental Biology 214, 131–146.CrossRefGoogle ScholarPubMed
Goldbogen, J.A., Calambokidis, J., Shadwick, R.E., Oleson, E.M., McDonald, M.A. & Hildebrand, J.A. (2006). Kinematics of foraging dives and lunge-feeding in fin whales. The Journal of Experimental Biology 209, 1231–1244.CrossRefGoogle ScholarPubMed
Goodyear, J.D. (1993). A sonic/radio tag for monitoring dive depths and underwater movements of whales. The Journal of Wildlife Management 57, 503–513.CrossRefGoogle Scholar
Govardovskii, V.I., Fyhrquist, N., Reuter, T., Kuzmin, D.G. & Donner, K. (2000). In search of the visual pigment template. Visual Neuroscience 17, 509–528.CrossRefGoogle ScholarPubMed
Hunt, D.M., Fitzgibbon, J., Slobodyanyuk, S.J. & Bowmaker, J.K. (1996). Spectral tuning and molecular evolution of rod visual pigments in the species flock of cottoid fish in Lake Baikal. Vision Research 36, 1217–1224.CrossRefGoogle ScholarPubMed
Lavigne, D.M. & Ronald, K. (1975). Pinniped visual pigments. Comparative Biochemistry and Physiology. Part B, Biochemistry and Molecular Biology 52, 325–329.CrossRefGoogle ScholarPubMed
Lythgoe, J.N. & Dartnall, H.J. (1970). A “deep sea rhodopsin” in a mammal. Nature 227, 955–956.CrossRefGoogle Scholar
Lythgoe, J.N. & Partridge, J.C. (1989). Visual pigments and the acquisition of visual information. The Journal of Experimental Biology 146, 1–20.CrossRefGoogle ScholarPubMed
Mathies, R. & Stryer, L. (1976). Retinal has a highly dipolar vertically excited singlet state: Implications for vision. Proceedings of the National Academy of Sciences of the United States of America 73, 2169–2173.CrossRefGoogle Scholar
McFarland, W.N. (1971). Cetacean visual pigments. Vision Research 11, 1065–1076.CrossRefGoogle ScholarPubMed
McGowen, M.R., Spaulding, M. & Gatesy, J. (2009). Divergence date estimation and a comprehensive molecular tree of extant cetaceans. Molecular Phylogenetics and Evolution 53, 891–906.CrossRefGoogle Scholar
Meier, S.K., Yazvenko, S.B., Blokhin, S.A., Wainwright, P., Maminov, M.K., Yakovlev, Y.M. & Newcomer, M.W. (2007). Distribution and abundance of western gray whales off northeastern Sakhalin Island, Russia, 2001-2003. Environmental Monitoring and Assessment 134, 107–136.CrossRefGoogle ScholarPubMed
Merbs, S. & Nathans, J. (1993). Role of hydroxyl-bearing amino acids in differentially tuning the absorption spectra of the human red and green cone pigments. Photochemistry and Photobiology 58, 706–710.CrossRefGoogle ScholarPubMed
Molday, R.S. & MacKenzie, D. (1983). Monoclonal antibodies to rhodopsin: Characterization, cross-reactivity, and application as structural probes. Biochemistry 22, 653–660.CrossRefGoogle ScholarPubMed
Nakayama, T.A. & Khorana, H.G. (1991). Mapping of the amino acids in membrane-embedded helices that interact with the retinal chromophore in bovine rhodopsin. The Journal of Biological Chemistry 266, 4269–4275.CrossRefGoogle ScholarPubMed
Nathans, J. (1990). Determinants of visual pigment absorbance: Role of charged amino acids in the putative transmembrane segments. Biochemistry 29, 937–942.CrossRefGoogle ScholarPubMed
Newman, L. & Robinson, P. (2005). Cone visual pigments of aquatic mammals. Visual Neuroscience 22, 873–879.CrossRefGoogle ScholarPubMed
Nickle, B., Wilkie, S.E., Cowing, J.A., Hunt, D.M. & Robinson, P.R. (2006). Vertebrate opsins belonging to different classes vary in constitutively active properties resulting from salt-bridge mutations. Biochemistry 45, 7307–7313.CrossRefGoogle ScholarPubMed
Norris, K.S. (1969). Echolocation of marine mammals. In The Biology of Marine Mammals, ed. Anderson, H.T., pp. 391–423. New York: Academic Press.Google Scholar
Nowacek, D.P., Friedlaender, A.S., Halpin, P.N., Hazen, E.L., Johnston, D.W., Read, A.J., Espinasse, B., Zhou, M. & Zhu, Y. (2011). Super-aggregations of krill and humpback whales in Wilhelmina Bay, Antarctic Peninsula. PLoS One 6, e19173.CrossRefGoogle ScholarPubMed
Palczewski, K., Kumasaka, T., Hori, T., Behnke, C.A., Motoshima, H., Fox, B.A., Le Trong, I., Teller, D.C., Okada, T., Stenkamp, R.E., Yamamoto, M. & Miyano, M. (2000). Crystal structure of rhodopsin: A G protein-coupled receptor. Science 289, 739–745.CrossRefGoogle ScholarPubMed
Panigada, S., Zanardelli, M., Canese, S. & Jahoda, M. (1999). How deep can baleen whales dive? Marine Ecology Progress Series 187, 309–311.CrossRefGoogle Scholar
Piggins, D., Muntz, W.R.A. & Best, R.C. (1983). Physical and morphological aspects of the eye of the manatee Trichechus inunquis Natterer 1883: (Sirenia: mammalia). Marine Behaviour and Physiology 9, 19.CrossRefGoogle Scholar
Pyenson, N.D. & Lindberg, D.R. (2011). What happened to gray whales during the Pleistocene? The ecological impact of sea-level change on benthic feeding areas in the North Pacific Ocean. PLoS One 6, e21295.CrossRefGoogle ScholarPubMed
Tyack, P.L., Johnson, M., Soto, N.A., Sturlese, A. & Madsen, P.T. (2006). Extreme diving of beaked whales. The Journal of Experimental Biology 209, 4238–4253.CrossRefGoogle ScholarPubMed
Watkins, W.A., Daher, M.A., Fristrup, K.M. & Howald, T.J. (1993). Sperm whales tagged with transponders and tracked underwater by sonar. Marine Mammal Science 9, 55–67.CrossRefGoogle Scholar
Watwood, S.L., Miller, P.J., Johnson, M., Madsen, P.T. & Tyack, P.L. (2006). Deep-diving foraging behaviour of sperm whales (Physeter macrocephalus). The Journal of Animal Ecology 75, 814–825.CrossRefGoogle ScholarPubMed
Werth, A.J. (2004). Models of hydrodynamic flow in the bowhead whale filter feeding apparatus. The Journal of Experimental Biology 207, 3569–3580.CrossRefGoogle ScholarPubMed
Winn, H., Goodyear, J., Kenney, R. & Petricig, R. (1995). Dive patterns of tagged right-whales in the great south channel. Continental Shelf Research 15, 593–611.CrossRefGoogle Scholar
Xie, G., Gross, A.K. & Oprian, D.D. (2003). An opsin mutant with increased thermal stability. Biochemistry 42, 1995–2001.CrossRefGoogle ScholarPubMed
Yokoyama, S. (2008). Evolution of dim-light and color vision pigments. Annual Reviews Genomics and Human Genetics 9, 259–282.CrossRefGoogle ScholarPubMed
Zhukovsky, E. & Oprian, D. (1989). Effect of carboxylic acid side chains on the absorption maximum of visual pigments. Science 246, 928–930.CrossRefGoogle ScholarPubMed