Skip to main content
Log in

Radular myoglobin and protein variation within and among some littorinid species (Mollusca: Gastropoda)

  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

The radular muscles of several littorinid species, including Littorina littorea, L. saxatilis, L. obtusata, L. striata and Melarhaphe neritoides, contain myoglobin (Mb). Here we report on the presence of radular Mb in eight other littorinids: L. compressa, L. arcana, L. fabalis, Nodilittorina punctata, N. trochoides, N. radiata, Littoraria undulata and Littoraria cingulifera. Using native polyacrylamide gel electrophoresis (PAGE) and isoelectric focusing (IEF) we compared the Mb and soluble protein (SP) profiles of these species. This suggested that: (1) L. saxatilis and L. arcana may have specific Mb/SP profiles, (2) Littoraria spp., Nodilittorina spp. and L. striata share similar Mb patterns, (3) Mb is remarkably diverse in the genus Littorina, (4) L. littorea shows intraspecific Mb/SP variation, (5) L. saxatilis does not show geographic Mb/SP differences, and (6) IEF uncovers substantial hidden Mb/SP heterogeneity not shown by PAGE (particularly for Melarhaphe neritoides). Hence, littorinid Mb/SP may be a useful taxonomic marker whose ecophysiological significance deserves further study, even if its genetic basis remains unclear.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Alexandrino, P. J., N. Ferrand & J. Rocha, 1996. Genetic polymorphism of a haemoglobin chain and adenosine deaminase in European shads: evidence for the existence of two distinct genetic entities with natural hybridization. J. Fish Biol. 48: 447–456.

    Google Scholar 

  • Alyakrinskaya, I. O., 1986. Hemoglobin content in subradular cartilages of the gastropod mollusc Littorina littorea. Zh. Evol. Biokhim. Fisiol. 22: 575–577. [in Russian].

    Google Scholar 

  • Alyakrinskaya, I. O., 1989. Biochemical adaptations of some littoral molluscs to feeding. Zh. Evol. Biokhim. Fisiol. 25: 112–115. [in Russian].

    Google Scholar 

  • Alyakrinskaya, I. O., 1994. Haemoglobin concentration and its functional meaning in White Sea Littorina. Gidrobiol. Zh. 30: 69–78. [in Russian].

    Google Scholar 

  • Atassi, M. Z., 1964. Properties of components of myoglobin of the sperm whale. Nature 202: 496–498.

    Google Scholar 

  • Backeljau, T., 1989. Electrophoresis of albumen gland proteins as a tool to elucidate taxonomic problems in the genus Arion (Gastropoda, Pulmonata). J. med. appl. malacol. 1: 29–41.

    Google Scholar 

  • Backeljau, T. & T. Warmoes, 1992. The phylogenetic relationships of ten Atlantic littorinids assessed by allozyme electrophoresis. In J. Grahame, P. J. Mill & D. G. Reid (eds), Proceedings of the Third International Symposium on Littorinid Biology. The Malacological Society of London, London: 9–24.

    Google Scholar 

  • Backeljau, T., K. Breugelmans, H. Leirs, T. Rodriguez, D. Sherbakov, T. Sitnikova, J.-M. Timmermans, J. L. Van Goethem & E. Verheyen, 1994. Application of isoelectric focusing in molluscan systematics. The Nautilus, Suppl. 2: 156–167.

    Google Scholar 

  • Bailey, J. B., E. H. Michelson & W. L. Paraense, 1986. Differentiation of the sibling species Biomphalaria occidentalis and Biomphalaria tenagophila by the electrophoretic patterns of their hemoglobin. Mem. Inst. Oswaldo Cruz 81: 319–322.

    Google Scholar 

  • Bannister, W. H., J. V. Bannister & H. Micallef, 1968. Occurrence of haemoglobin in the radular muscles of some prosobranch molluscs. Comp. Biochem. Physiol. 24: 1061–1063.

    Google Scholar 

  • Basaglia, F. & C. Callegarini, 1987. Electrophoretic and isoelectrophoretic characteristics of hemoglobins of Italian ictalurids. Comp. Biochem. Physiol. 86B: 269–271.

    Google Scholar 

  • Berger, E., 1977. Gene-enzyme variation in three sympatric species of Littorina. II. The Roscoff population, with a note on the origin of North American L. littorea. Biol. Bull. 153: 255–264.

    Google Scholar 

  • Bonaventura, C. & J. Bonaventura, 1983. Respiratory pigments: structure and function. In K. M. Wilbur & P. W. Hochachka, (eds), The Mollusca, Volume 2, Environmental Biochemistry and Physiology. Academic Press, New York: 1–50.

    Google Scholar 

  • Bonaventura, J., C. Bonaventura & B. Sullivan, 1975. Hemoglobins and hemocyanins: comparative aspects of structure and function. J. exp. Zool. 194: 155–174.

    Google Scholar 

  • Broyles, R. H., B. M. Pack, S. Berger & A. R. Dorn, 1979. Quantification of small amounts of hemoglobin in polyacrylamide gels with benzidine. Analyt. Biochem. 94: 211–219.

    Google Scholar 

  • Das, R. & R. Handique, 1996. Hemoglobin in Chironomus ramosus (Insecta, Diptera): an electrophoretic study of polymorphism, developmental sequence and interspecific relationship. Hydrobiologia 318: 43–50.

    Google Scholar 

  • Edmundson, A. B. & C. H.W. Hirs, 1962. On the structure of sperm whale myoglobin I. The amino acid composition and terminal groups of the chromatographically purified protein. J. Mol. Biol. 5: 663–682.

    Google Scholar 

  • Giraldino, I., M. C. Pico & R. Alegre, 1995. Mioglobina humana: aislamiento y purificacion. Rev. Biol. 9: 23–29.

    Google Scholar 

  • Johannesson, K., 1992. Genetic variability and large scale differentiation in two species of littorinid gastropods with planktotrophic development, Littorina littorea (L.) and Melarhaphe (Littorina) neritoides (L.) (Prosobranchia: Littorinacea), with notes on a mass occurrence of M. neritoides in Sweden. Biol. J. linn. Soc. 47: 285–299.

    Google Scholar 

  • Jones, M. L., 1972. Comparisons of electrophoretic patterns of littorine snails of Panama: an attempt to define geminate species. XVIIe Congrès International de Zoologie, Monte Carlo, 25–30 Septembre 1972, Thème 3: 1–10.

    Google Scholar 

  • Lavrenchenko, L. A., O. P. Kihnova & V. N. Orlov, 1992. Hemoglobin patterns: a possible implication in systematics of multimammate rats Mastomys (Muridae, Rodentia). Zool. Zh. 71: 85–93. [in Russian].

    Google Scholar 

  • Macaranas, J. M., L. Q. Agustin & A. E. Eknath, 1996. Multiple haemoglobins in three tilapiine species of the genus Oreochromis and in eight strains of O. niloticus (L.). Aquacult. Res. 27: 597– 601.

    Google Scholar 

  • Mangum, C. P., 1996. Subunit composition of polymorphic hemocyanins in the decapod crustaceans: differences between sibling species. Physiol. Zool. 69: 568–585.

    Google Scholar 

  • Mangum, C. P. & J. Greaves, 1996. Hemocyanins of the genus Uca: structural polymorphisms and native oligomers. J. exp. mar. Biol. Ecol. 199: 1–15.

    Google Scholar 

  • Mangum, C. P. & A. L. McKenney, 1996. Subunit composition of the crustacean hemocyanins: divergence in incipient speciation. Biol. Bull. 191: 33–41.

    Google Scholar 

  • Mulvey, M., M. C. Newman & D. S. Woodruff, 1988. Genetic differentiation among west Indian populations of the schistosometransmitting snail Biomphalaria glabrata. Malacologia 29: 309–317.

    Google Scholar 

  • O'Gower, A. K. & P. I. Nicol, 1968. A latitudinal cline of haemoglobins in a bivalve mollusc. Heredity 23: 485–491.

    Google Scholar 

  • Olabarria, C., J.-M. Timmermans & T. Backeljau, 1998. Electrophoretic heterogeneity within and between flat periwinkles (Mollusca: Gastropoda) along an intertidal transect at Ria Ferrol, northwest Spain. Hydrobiologia 378: 11–19.

    Google Scholar 

  • Olsson, I., U.-B. Axio-Fredriksson, M. Degerman, & B. Olsson, 1988. Fast horizontal electrophoresis. I. Isoelectric focusing and polyacrylamide gel electrophoresis using Phastsystem. Electrophoresis 9: 16–22.

    Google Scholar 

  • Parkhurst, L. J. & J. LaGow, 1975. Kinetic and equilibrium studies of the ligand binding reactions of eight electrophoretic components of sperm whale ferrimyoglobin. Biochemistry 14: 1200–1205.

    Google Scholar 

  • Read, K. R. H., 1966. Molluscan hemoglobin and myoglobin. In K. M. Wilbur & C. M. Yonge (eds), Physiology of Mollusca, Volume II. Academic Press, New York: 209–232.

    Google Scholar 

  • Read, K. R. H., 1968. The myoglobins of the gastropod molluscs Busycon contrarium Conrad, Lunatia heros Say, Littorina littorea L. and Siphonaria gigas Sowerby. Comp. Biochem. Physiol. 25: 81–94.

    Google Scholar 

  • Reid, D. G., 1986. The littorinid molluscs of mangrove forests in the Indo-Pacific region. British Museum (Natural History), London. 228 pp.

    Google Scholar 

  • Reid, D. G., 1989. The comparative morphology, phylogeny and evolution of the gastropod family Littorinidae. Phil. Trans. r. Soc. Lond. B 324: 1–110.

    Google Scholar 

  • Reid, D. G., 1990. A cladistic phylogeny of the genus Littorina (Gastropoda): implications for evolution of reproductive strategies and for classification. Hydrobiologia 193: 1–19.

    Google Scholar 

  • Reid, D. G., 1992. The gastropod family Littorinidae in Hong Kong. In B. Morton (ed.), The Marine Flora and Fauna of Hong Kong and Southern China III. Hong Kong University Press, Hong Kong: 187–210.

    Google Scholar 

  • Reid, D. G., 1996. Systematics and evolution of Littorina. The Ray Society, London. 463 pp.

    Google Scholar 

  • Reid, D. G., E. Rumbak & R. H. Thomas, 1996. DNA, morphology and fossils: phylogeny and evolutionary rates of the gastropod genus Littorina. Phil. Trans. r. Soc. Lond. B 351: 877–895.

    Google Scholar 

  • Riggs, A., 1981. Preparation of the blood hemoglobins of vertebrates. Meth. Enzym. 76: 5–29.

    Google Scholar 

  • Righetti, P. G., 1983. Isoelectric focusing: theory, methodology and applications. Elsevier, Amsterdam. 386 pp.

    Google Scholar 

  • Rumen, N. M., 1959. Isolation of five myoglobins from seal (Phoca vitulina). Acta Chem. Scand. 13: 1542–1546.

    Google Scholar 

  • Symondson, W. O. C. & M. P. Walton, 1994. Electrophoretic separation of pulmonate haemocyanins: a simple taxonomic tool. J. moll. Stud. 60: 351–354.

    Google Scholar 

  • Terwilliger, R. C. & R. H. Read, 1969. The radular muscle myoglobins of the amphineuran mollusc, Acanthopleura granulata Gmelin. Comp. Biochem. Physiol. 29: 551–560.

    Google Scholar 

  • Wittenberg, J. B. & B. A. Wittenberg, 1981. Preparation of myoglobins. Meth. Enzymol. 76: 29–42.

    Google Scholar 

  • Wium-Andersen, G., 1970. Haemoglobin and protein variation in three species of Littorina. Ophelia 8: 267–273.

    Google Scholar 

  • Woodruff, D. S. & M. Mulvey, 1997. Neotropical schistosomiasis: African affinities of the host snail Biomphalaria glabrata (Gastropoda: Planorbidae). Biol. J. linn. Soc. 60: 505–516.

    Google Scholar 

Download references

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Medeiros, R., Serpa, L., Brito, C. et al. Radular myoglobin and protein variation within and among some littorinid species (Mollusca: Gastropoda). Hydrobiologia 378, 43–51 (1998). https://doi.org/10.1023/A:1003273101855

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1003273101855

Navigation