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Studies on the haemoglobins of the small Pogonophora

Published online by Cambridge University Press:  11 May 2009

R. C. Terwilliger ,
N. B. Terwilliger ,
G. M. Hughes† ,
A. J. Southward†  and
E. C. Southward†
R. C. Terwilliger
Affiliation:
Oregon Institute of Marine Biology, University of Oregon, Charleston, OR 97410, U.S.A.
N. B. Terwilliger
Affiliation:
Oregon Institute of Marine Biology, University of Oregon, Charleston, OR 97410, U.S.A.
G. M. Hughes†
Affiliation:
Research Unit for Comparative Animal Respiration, The University, Bristol BS8 1UG
A. J. Southward†
Affiliation:
The Laboratory, Marine Biological Association, Citadel Hill, Plymouth PL1 2PB
E. C. Southward†
Affiliation:
The Laboratory, Marine Biological Association, Citadel Hill, Plymouth PL1 2PB
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Abstract

Haemoglobin is present, often at high concentration, dissolved in the blood of all small Pogonophora so far examined.

The haemoblobin of Siboglinum fiordicum resembles annelid and vestimentiferan haemoglobins in having subunits with molecular weights of 15000–16700 plus traces of 35000–40000 MW material. 5. fiordicum haemoglobin has 1 mol haem per 21500 g protein, and a similar lack of correspondence between subunits and mols of haem is shown by annelid and vestimentiferan haemoglobins. However, S. fiordicum haemoglobin differs considerably from annelid and vestimentiferan haemoglobins in other respects, even though the three groups are closely linked taxonomically. The haemoglobin of S. fiordicum has a lower apparent molecular weight (Mr = 3.5–4.0 x 105) than that of annelid haemoglobins (Mr = 3–4 x 108) when measured under the same conditions. Pogonophore blood examined with the electron microscope does not show the two-tiered hexagonal structure found in annelid and vestimentiferan haemoglobins. S. fiordicum haemoglobin also differs from annelid and vestimentiferan haemoglobins in amino acid composition.

The haemoglobins of the small pogonophores examined have a very high affinity for oxygen. The P 50 ranges from 0.36 Torr in diluted blood of S. fiordicum (15 °C) to 0.5–1.0 Torr in undiluted blood of S. atlanticum (10 °C) and s. fiordicum (15 °C). Only a slight Bohr effect was found. The high oxygen affinity can be related to the wide range of P o2 values experienced in the habitat and the need to transport oxygen to the deeply buried posterior end of the body that contains autotrophic endosymbiotic bacteria.

Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 67 , Issue 1 , February 1987 , pp. 219 - 234
Copyright
Copyright © Marine Biological Association of the United Kingdom 1987

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References

Antonini, E. & Chiancone, E., 1977. Assembly of multisubunit respiratory proteins. Annual Review of Biophysics and Bioengineering, 6, 239–271.CrossRefGoogle ScholarPubMed
Arp, A. & Childress, J. J., 1981. Blood function in the hydrothermal vent vestimentiferan worm. Science, New York, 213, 342–344.CrossRefGoogle Scholar
Benesch, R., Macduff, G. & Benesch, R. E., 1965. Determination of oxygen equilibrium with a versatile new tonometer. Analytical Biochemistry, 11, 81–87.CrossRefGoogle Scholar
Brenner, S. & Horne, R. W., 1959. A negative staining method for high resolution electron mocroscopy of viruses. Biochemica et biophysica acta, 34, 103–110.CrossRefGoogle Scholar
Dando, P. R., Southward, A. J., Southward, E. C. & Barrett, R. L., 1986. Possible energy sources for chemoautotrophic prokaryotes symbiotic with invertebrates from a Norwegian fjord. Ophelia, in press.CrossRefGoogle Scholar
Dando, P. R., Southward, A. J., Southward, E. C., Terwilliger, N. B. & Terwilliger, R. C., 1985. Sulphur-oxidising bacteria and haemoglobin in gills of the bivalve mollusc Myrtea spinifera. Marine Ecology-Progress Series, 23, 85–98.CrossRefGoogle Scholar
Davis, B., 1964. Disc gel electrophoresis-II. Method and application to human serum proteins. Annals of the New York Academy of Sciences, 121, 404–427.CrossRefGoogle Scholar
Garlick, R. & Riggs, A., 1982. The amino acid sequence of a major polypeptide chain of earthworm hemoglobin. Journal of Biological Chemistry, 257, 9005–9015.CrossRefGoogle Scholar
Harris, C. E. & Teller, D. C., 1973. Estimates of primary sequence homology from amino acid composition of evolutionary related proteins. Journal of Theoretical Biology, 38, 347–362.CrossRefGoogle ScholarPubMed
Haschmeyer, R. H. & Myers, R. J., 1972. Negative staining. In Principles and Techniques of Electron Microscopy, vol. 2 (ed. Hayat, M. A.), pp. 101–147. New York: Van Nostrand Reinhold Co.Google Scholar
Jones, M. L., 1980. Riftia pachyptila, new genus, new species, the vestimentiferan worm from the Galapagos Rift geothermal vents (Pogonophora). Proceedings of the Biological Society of Washington, 93, 1295–1313.Google Scholar
Jones, M., 1981. Riftia pachyptila Jones: observations on the vestimentiferan worm from the Galapagos Rift. Science, New York, 213, 333–336.CrossRefGoogle ScholarPubMed
Jones, H., 1985. On the Vestimentifera, new phylum: six new species and other taxa, from hydrothermal vents and elsewhere. Bulletin of the Biological Society of Washington, no. 6, 117–158.Google Scholar
Laemmli, U. K., 1970. Cleavage of structural proteins during the assembly of the head of the bacteriophage T4. Nature, London, 227, 670–685.CrossRefGoogle ScholarPubMed
Lapennas, B. N., Colacino, J. M. & Bonaventura, J., 1981. Then layer methods for determination of oxygen binding curves by hemoglobin solutions and red blood cells. In Methods in Enzymology, vol. 76 (ed. Antonini, A. E., Rossi-Bernardi, L. and Chiancone, E.), pp. 449–470. New York: Academic Press.Google Scholar
Manwell, C., Southward, E. C. & Southward, A. J., 1966. Preliminary studies on haemoglobin and other proteins of the Pogonophora. Journal of the N'arine Biological Association of the United Kingdom, 46, 115–124.Google Scholar
Perutz, M., 1983. Species adaptation in a protein molecule. Molecular Biology and Evolution, 1, 1–28.Google ScholarPubMed
Royer, W. E., Love, W. E. & Fenderson, F. F., 1985. Narative dimeric and tetrameric clam haemoglobins are novel assemblages of myoglobin form. Nature, London, 316, 277–280.CrossRefGoogle Scholar
Southward, A. J. & Dixon, D. R., 1980. A note on the manifio acids in some small species of Pogonophora. Journal of the Marine Biological Association of the United Kingdom, 60, 171–174.CrossRefGoogle Scholar
Southward, A. J. & Southward, E. C., 1963. Notes on the biology of some Pogonophora. Journal of the Marine Biological Association of the United Kingdom, 43, 57–64.CrossRefGoogle Scholar
Southward, A. J., Southward, E. C., Brattegard, T. & Bakke, T., 1979. Further experiments on the value of dissolved organic matter as food for Siboglihum fiordicum (Pogonophora). Journal of the Marine Biological Association of the United Kingdom, 59, 133–148.CrossRefGoogle Scholar
Southward, A. J., Southward, E. C., Dando, P. R., Barrett, R. L. & Ling, R., 1986. Chemoautotrophic function of bacterial symbionts in small Pogonophora. Journal of the Marine Biological Association of the United Kingdom, 66, 415–437.CrossRefGoogle Scholar
Southward, E. C., 1975. Fine structure and phylogeny of the Pogonophora. Symposia of the Zoological Society of London, no. 36, 235–251.Google Scholar
Spackman, D., Stein, W. & Moore, S., 1958. Automatic recording apparatus for use in chromatography of amino acids. Analytical Chemistry, 30, 1190–1206.CrossRefGoogle Scholar
Suzuki, R., Furokhori, R. & Gotoh, T., 1985. Subunit structure of extracellular hemoglobin from the polychaete Tylorrhynchus heterochaetus and amino acid sequence of the constituent polypeptide chain (11C). Journal of Biological Chemistry, 260, 3145–3154.CrossRefGoogle Scholar
Terwilliger, N. B. & Terwilliger, R. C., 1981. Structural similarity between extracellular hemoglobin from a deep sea Vestimentifera and annelids. In Invertebrate Oxygen Binding Proteins, Structure, Active Site and Function (ed. Lamy, J. and Lamy, J.), pp. 369–371. Marcel Dekker.Google Scholar
Terwilliger, R. C., 1980. Structures of invertebrate hemoglobins. American Zoologist, 20, 53–67.CrossRefGoogle Scholar
Terwilliger, R. C. & Terwilliger, N. B., 1983. Oxygen binding domains in invertebrate hemoglobins. In Structure and Function of Invertebrate Respiratory Proteins (ed. Wood, E. J.), pp. 227–238. Great Britain: Harwood Academic Publishers.Google Scholar
Terwilliger, R. C. & Terwilliger, N. B., 1985. Respiratory proteins of hydrothermal vent animals. Bulletin of the Biological Society of Washington, no. 6, 273–287.Google Scholar
Terwilliger, R. C., Terwilliger, N. B. & Roxby, R. L., 1975. Quaternary structure of Pista pacifica vascular hemoglobin. Comparative Biochemistry and Physiology, 50 B, 225–232.Google ScholarPubMed
Terwilliger, R. C., Terwilliger, N. B. & Schabtach, E. 1980. The structure of hemoglobin from an unusual deep sea worm (Vestimentifera). Comparative Biochemistry and Physiology, 65B, 531–535.Google Scholar
Terwilliger, R. C., Terwilliger, N., Bonaventura, C., Bonaventura, J. & Schabtach, E., 1985. Structural and functional properties of hemoglobin from the vestimentiferan Pogonophora Lamellibrachia. Biochimica et biophysica acta, 829, 27–33.CrossRefGoogle Scholar
Van Assendelft, O. W. & Zijlstra, W. G., 1975 Extinction coefficients for use in equations for the spectrophotometric analysis of hemoglobin mixtures. Analytical Biochemistry, 69, 43–48.CrossRefGoogle Scholar
Van Holde, K. & Miller, K., 1982. Haemocyanins. Quarterly Review of Biophysics, 15, 1–129.CrossRefGoogle ScholarPubMed
Vinogradov, S., 1985. The structure of erythrocruorins and chlorocruorins, the invertebrate extracellular hemoglobins. In Respiratory Pigments in Animals (ed. Lamy, J., Truchot, J. P. and Gilles, R.), pp. 9–20. Berlin: Springer.CrossRefGoogle Scholar
Vinogradov, S. N., Hall, B. C. & Schlom, J. M., 1976. Subunit homology in invertebrate hemoglobins: a primitive heme binding chain? Comparative Biochemistry and Physiology, 53 B, 89–92.Google ScholarPubMed
Vinogradov, S., Schlom, J. & Ohtsuki, M., 1982. The extracellular hemoglobins and chlorocruorins of annelids. In Electron Microscopy of Proteins (ed. Harris, J.), vol. 3, pp. 135—164. London: Academic Press.Google Scholar
Webb, M., 1969. Lamellibrachia barhami, gen.nov., sp.nov. (Pogonophora), from the northeast Pacific. Bulletin of Marine Science, 19, 18–47.Google Scholar
Wells, R. M. & Dales, R. P., 1976. A preliminary investigation into the oxygen combining properties of pogonophore haemoglobin. Comparative Biochemistry and Physiology, 54A, 395–396.CrossRefGoogle ScholarPubMed