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Oxygen and carbon dioxide transporting qualities of hemocyanin in the hemolymph of a natant decapodPalaemon adspersus

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Summary

  1. 1.

    The O2 and CO2 combining properties ofPalaemon adspersus hemolymph is studied, aiming to assess respiratory function and the environmental and metabolic adaptations of hemocyanin of natant decapods where, in contrast to the intensively-studied, larger and predominantly less active reptant decapods, virtually no information is available.

  2. 2.

    The hemolymph shows a high O2 carrying capacity (mean=2.8 vol%), a low O2 affinity (at 15 °C half-saturation tension,P 50=16 and 37 mm Hg at pH 7.85 and 7.65, respectively), pronounced cooperativity in O2 binding (Hill's coefficient,n≃2.8) and a large, pH dependent Bohr factor (ϕ=ΔlogP 50/ΔpH=−2.0 and −0.9 at pH 7.85 and 7.4, respectively) (Figs. 1 and 2). These qualities are distinct from those typifying reptant hemocyanins and appear illsuited for O2 transport at low ambient tensions, but well-adapted for O2 delivery in tissues at highP O 2, supporting high levels of metabolism and activity.

  3. 3.

    CO2 has a specific, augmenting effect on O2 affinity at high pH (Fig. 3), indicating carbamate formation with an opposite oxygenation-linkage as in vertebrate hemoglobins. Astrup titrations indicate the presence of a small but distinct Haldane effect at physiological pH, and buffering capacity varies greatly (ΔHCO3/ΔpH≃−4.4 to −9.3 mmol·1−1·(pH unit)−1 depending on hemocyanin concentration) (Fig. 4). Equilibrium curves of total, non-protein-bound CO2 show large capacitance for transport at low, in vivo CO2 tensions (Fig. 4).

  4. 4.

    The data are discussed comparatively, particularly as regards hemocyanin function in reptant decapods, and the O2, CO2 and proton exchanges involved.

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References

  • Ainslie RC (1980) The quantitative role of haemocyanin in the respiration of abalone (genusHaliotis). J Exp Zool 211:87–99

    Google Scholar 

  • Angersbach, D, Decker H (1978) Oxygen transport in crayfish blood: Effect of thermal acclimation, and short-term fluctuations related to ventilation and cardiac performance. J Comp Physiol 123:105–112

    Google Scholar 

  • Boone WR, Schoffeniels E (1979) Hemocyanin synthesis during hypo-osmotic stress in the shore crabCarcinus maenas (L.). Comp Biochem Physiol 63B:207–214

    Google Scholar 

  • Bridges CR, Bicudo JEPW, Lykkeboe G (1979) Oxygen content measurement in blood containing haemocyanin. Comp Biochem Physiol 62A:457–462

    Google Scholar 

  • Burnett LE (1979) The effects of environmental oxygen levels on the respiratory function of hemocyanin in the crabsLibinia emarginata andOcypode quadrata. J Exp Zool 210:289–299

    Google Scholar 

  • Busselen P (1970). Effects of moulting cycle and nutritional conditions on haemolymph proteins inCarcinus maenas. Comp Biochem Physiol 37:73–83

    Google Scholar 

  • Cook SF (1927) The action of potassium cyanide and potassium ferricyanide on certain respiratory pigments. J Gen Physiol 11:339–346

    Google Scholar 

  • Djangmah JS (1970a) The effects of feeding and starvation on copper in the blood and hepatopancreas, and on blood proteins ofCrangon vulgaris (Fabricius). Comp Biochem Physiol 32:709–731

    Google Scholar 

  • Djangmah JS (1970b) Blood and hepatopancreas copper inCrangon vulgaris (Fabricius). Comp Biochem Physiol 32:733–745

    Google Scholar 

  • Hagerman L, Uglow RF (1979) Heart and scaphognathite activity in the shrimpPalaemon adspersus Rathke. Ophelia 18:89–96

    Google Scholar 

  • Hagerman L, Weber RE (1981) Respiratory rate, hemolymph oxygen tension and hemocyanin level in the shrimpPalaemon adspersus Rathke. J Exp Mar Biol Ecol 54:13–20

    Google Scholar 

  • Johansen K, Lenfant C, Anthony-Mecklenburg T (1970) Respiration in the crab,Cancer magister. Z Vergl Physiol 70:1–19

    Google Scholar 

  • Krogh-Rasmussen K, Weber RE (1979) Respiratory properties of erythrocruorin (extracellular hemoglobin) in the blood of the annelidArenicola marina with special reference to the influences of salinity and temperature. Ophelia 18:151–170

    Google Scholar 

  • Lontie R, Witters R (1973) Hemocyanin. In: Eichhorn GL (ed) Inorganic biochemicstry. Elsevier, Amsterdam, pp 344–358

    Google Scholar 

  • Lykkeboe G, Brix O, Johansen K (1980) Oxygen-linked CO2 binding independent of pH in cephalopod blood. Nature 287:330–331

    Google Scholar 

  • Mangum CP (1980) Respiratory function of hemocyanins. Am Zool 20:19–38

    Google Scholar 

  • Mangum CP, Lykkeboe L (1979) The influence of inorganic ions and pH on oxygenation properties of the blood in the gastropod molluscBusycon canaliculatum. J Exp Zool 207:417–430

    Google Scholar 

  • Mangum CP, Shick JM (1972) The pH of body fluids of marine invertebrates. Comp Physiol Biochem 42A:693–697

    Google Scholar 

  • Mangum CP, Weiland AL (1975) Function of hemocyanin in respiration of the blue crabCallinectes sapidus. J Exp Zool 193:257–264

    Google Scholar 

  • Mauro NA (1978) The effect of temperature on oxygen transport in decapod crustaceans. Am Zool 18:639

    Google Scholar 

  • McMahon BR, McDonald DG, Wood CM (1979) Ventilation, oxygen uptake and haemolymph oxygen transport following enforced exhausting activity in the Dungeness crabCancer magister. J Exp Biol 80:271–285

    Google Scholar 

  • Miller K, Holde KE Van (1974) Oxygen binding byCallianassa californiensis hemocyanin. Biochemistry 13:1668–1674

    Google Scholar 

  • Miller KI, Pritchard AW, Rutledge PS (1976) Respiratory regulation and the role of the blood in the burrowing shrimpCallianassa californiensis (Decapoda, Thalassinidea). Mar Biol 36:233–242

    Google Scholar 

  • Miller KI, Eldred NW, Arisaka F, Holde KE Van (1977) Structure and function of hemocyanin from thalassinid shrimp. J Comp Physiol 115:171–184

    Google Scholar 

  • Muus B (1967) The fauna of the Danish estuaries and lagoons. Medd Dan Fisk Havunders NS 5:1–316

    Google Scholar 

  • Nickerson KW, Van Holde KE (1971) A comparison of molluscan and arthropod hemocyanin I. Circular dichroism and absorption spectra. Comp Biochem Physiol 39B:855–872

    Google Scholar 

  • Redmond JR (1968) The respiratory function of hemocyanin. In: Ghiretti F (ed) Physiology and biochemistry of hemocyanins. Academic Press, New York, pp 5–23

    Google Scholar 

  • Rossi-Bernardi L, Roughton EJW (1967) The specific influence of carbon dioxide and carbamate compounds in the buffer power and Bohr effects in human haemoglobin solutions. J Physiol 189:1–29

    Google Scholar 

  • Schoffeniels E (1976) Adaptations with respect to salinity. Biochem Soc Symp 41:179–204

    Google Scholar 

  • Sevilla C, Lagarrique J-G, (1979) Oxygen binding characteristics of Oniscoidea hemocyanins (Crustacea, terrestrial isopods). Comp Biochem Physiol 64A:531–536

    Google Scholar 

  • Sick H, Gersonde K (1969) Method for continuous registration of O2-binding curves of haemoproteins by means of a diffusion chamber. Anal Biochem 32:362–376

    Google Scholar 

  • Spoek GA (1962) Verslag van onderzoekingen gedaan in het Stazione Zoologica te Napels. K Ned Acad Wet (Amsterdam) 71:29–34

    Google Scholar 

  • Stadie WC, O'Brien H (1936) The carbamate equilibrium I. The equilibrium of amino acids, carbon dioxide and carbamates in aqueous solution with a note on the Ferguson-Roughton carbamate method. J Biol Chem 112:723–758

    Google Scholar 

  • Truchot J-P (1971a) Fixation de l'oxygène par le sérum deCarcinus maenas (L.) (Crustacé Décapode Brachyoure). CR Acad Sci (Paris) 272:984–987

    Google Scholar 

  • Truchot J-P (1971b) Etude comparée de la fixation de l'oxygène par le sérum de cinq espèces des Crustacés Décapodes Brachyoures. CR Acad Sci (Paris) 272:2706–2709

    Google Scholar 

  • Truchot J-P (1973a) Temperature and acid-base regulation in the shore crabCarcinus maenas (L.). Resp Physiol 17:11–20

    Google Scholar 

  • Truchot J-P (1973b) Action spécifique du dioxyde de carbone sur l'affinité pour l'oxygène de l'hémocyanine deCarcinus maenas (L.) (Crustacé Décapode Brachyoure). CR Acad Sci (Paris) 276:2965–2968

    Google Scholar 

  • Truchot J-P (1976a) Carbon dioxide combining properties of the blood of the shore crabCarcinus maenas (L.): Carbon dioxide solubility coefficient and carbonic acid dissociation constants. J Exp Biol 64:45–57

    Google Scholar 

  • Truchot J-P (1976b) Carbon dioxide combining properties of the blood of the shore crab,Carcinus maenas (L.): CO2-dissociation curves and the Haldane effect. J Comp Physiol 112:283–293

    Google Scholar 

  • Tucker VA (1967) Method for oxygen content and dissociation curves on microliter blood samples. J Appl Physiol 23:410–414

    Google Scholar 

  • Tyuma I, Ueda Y (1975) Non-linear relationship between oxygen saturation and proton release, and equivalence of the Bohr and Haldane effects in human hemoglobin. Biochem Biophys 64:1278–1283

    Google Scholar 

  • Uglow RF (1969) Haemolymph protein concentrations in Portunid crabs II. The effects of imposed fasting onCarcinus maenas. Comp Biochem Physiol 31:959–967

    Google Scholar 

  • Weber RE (1981) Cationic control of O2 affinity in lugworm erythrocruorin. Nature 292:386–387

    Google Scholar 

  • Weber RE, Hemmingsen EA, Johansen K (1974) Functional and biochemical studies of penguin myoglobin. Comp Biochem Physiol 49B:197–214

    Google Scholar 

  • Weber RE, Johansen K (1979) Oxygenation-linked binding of carbon dioxide and allosteric phosphate cofactors by lungfish hemoglobin. In: Gilles R (ed) Animals and environmental fitness. Pergamon Press, Oxford, pp 49–50

    Google Scholar 

  • Weber RE, Marrewijk JA van (1972) Free amino acids and the isosmotic intracellular regulation in the shrimpCrangon crangon. Life Sci 11:589–595

    Google Scholar 

  • Wolvekamp HP, Kruyt W (1948) Experiments on the carbon dioxide transport by the blood of the edible snail (Helix pomatia L.), the common crab (Cancer pagurus L.) and the common lobster (Homarus vulgaris ME). Arch Neerl Physiol 28:620–629

    Google Scholar 

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This work was supported by the Danish Natural Science Research Council. John Rosetti provided invaluable technical assistance

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Weber, R.E., Hagerman, L. Oxygen and carbon dioxide transporting qualities of hemocyanin in the hemolymph of a natant decapodPalaemon adspersus . J Comp Physiol B 145, 21–27 (1981). https://doi.org/10.1007/BF00782589

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