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Journal of Comparative Physiology B

, Volume 179, Issue 3, pp 369–381 | Cite as

Cationic composition and acid–base state of the extracellular fluid, and specific buffer value of hemoglobin from the branchiopod crustacean Triops cancriformis

  • Ralph Pirow
  • Ina Buchen
  • Marc Richter
  • Carsten Allmer
  • Frank Nunes
  • Andreas Günsel
  • Wiebke Heikens
  • Tobias Lamkemeyer
  • Björn M. von Reumont
  • Stefan K. Hetz
Original Paper
  • 122 Downloads

Abstract

Recent insights into the allosteric control of oxygen binding in the extracellular hemoglobin (Hb) of the tadpole shrimp Triops cancriformis raised the question about the physico-chemical properties of the protein’s native environment. This study determined the cationic composition and acid–base state of the animal’s extracellular fluid. The physiological concentrations of potential cationic effectors (calcium, magnesium) were more than one order of magnitude below the level effective to increase Hb oxygen affinity. The extracellular fluid in the pericardial space had a typical bicarbonate concentration of 7.6 mM but a remarkably high CO2 partial pressure of 1.36 kPa at pH 7.52 and 20°C. The discrepancy between this high CO2 partial pressure and the comparably low values for water-breathing decapods could not solely be explained by the hemolymph-sampling procedure but may additionally arise from differences in cardiovascular complexity and efficiency. T. cancriformis hemolymph had a non-bicarbonate buffer value of 2.1 meq L−1 pH−1. Hb covered 40–60% of the non-bicarbonate buffering power. The specific buffer value of Hb of 1.1 meq (mmol heme)−1 pH−1 suggested a minimum requirement of two titratable histidines per heme-binding domain, which is supported by available information from N-terminal sequencing and expressed sequence tags.

Keywords

Cationic composition Acid–base state Buffer value Hemolymph Hemoglobin Crustacea 

Notes

Acknowledgments

The authors would like to thank Rüdiger J. Paul for the general support of this project.

References

  1. Armougom F, Moretti S, Poirot O, Audic S, Dumas P, Schaeli B, Keduas V, Notredame C (2006) Expresso: automatic incorporation of structural information in multiple sequence alignments using 3D-Coffee. Nucleic Acids Res 34:W604–W608PubMedCrossRefGoogle Scholar
  2. Bennett-Lovsey RM, Herbert AD, Sternberg MJE, Kelley LA (2008) Exploring the extremes of sequence/structure space with ensemble fold recognition in the program Phyre. Proteins Struct Funct Bioinform 70:611–625CrossRefGoogle Scholar
  3. Berenbrink M (2006) Evolution of vertebrate haemoglobins: histidine side chains, specific buffer value and Bohr effect. Respir Physiol Neurobiol 154:165–184PubMedCrossRefGoogle Scholar
  4. Bhattacharya S, Lecomte JTJ (1997) Temperature dependence of histidine ionization constants in myoglobin. Biophys J 73:3241–3256PubMedCrossRefGoogle Scholar
  5. Burmester T (2002) Origin and evolution of arthropod hemocyanins and related proteins. J Comp Physiol B Biochem Syst Environ Physiol 172:95–107CrossRefGoogle Scholar
  6. Burton RF (1973) The roles of buffers in body fluids: mathematical analysis. Respir Physiol 18:34–42PubMedCrossRefGoogle Scholar
  7. Butler PJ, Taylor EW, McMahon BR (1978) Respiratory and circulatory changes in the lobster (Homarus vulgaris) during long term exposure to moderate hypoxia. J Exp Biol 73:131–146Google Scholar
  8. Cameron JN (1978) Effects of hypercapnia on blood acid-base status, NaCl fluxes, and trans-gill potential in freshwater blue crabs, Callinectes sapidus. J Comp Physiol 123:137–141Google Scholar
  9. Cohn EJ, Edsall JT (1943) Proteins, amino acids and peptides as ions and dipolar ions. Reinhold Publishing corporation, New YorkGoogle Scholar
  10. Dangott LJ, Terwilliger RC (1979) Structural studies of a branchiopod crustacean (Lepidurus bilobatus) extracellular hemoglobin: evidence for oxygen-binding domains. Biochim Biophys Acta 579:452–461PubMedGoogle Scholar
  11. Dangott LJ, Terwilliger RC (1981) Arthropod extracellular hemoglobins: Structural and functional properties. Comp Biochem Physiol B Biochem Mol Biol 70:549–557CrossRefGoogle Scholar
  12. Davies MN, Toseland CP, Moss DS, Flower DR (2006) Benchmarking pKa prediction. BMC Biochem 7:18PubMedCrossRefGoogle Scholar
  13. Duan Z, Sun R (2003) An improved model calculating CO2 solubility in pure water and aqueous NaCl solutions from 273 to 533 K and from 0 to 2000 bar. Chem Geol 193:257–271CrossRefGoogle Scholar
  14. Duan Z, Sun R, Zhu C, Chou I-M (2006) An improved model for the calculation of CO2 solubility in aqueous solutions containing Na+, K+, Ca2+, Mg2+, Cl-, and SO42-. Mar Chem 98:131–139CrossRefGoogle Scholar
  15. Fryer G (1988) Studies on the functional morphology and biology of the Notostraca (Crustacea, Branchiopoda). Philos Trans R Soc Lond B Biol Sci 321:27–127CrossRefGoogle Scholar
  16. Ghidalia W (1985) Structural and biological aspects of pigments. In: Bliss DE, Mantel LH (eds) The biology of crustacea: Integument, pigments, and hormonal responses Vol 9. Academic Press, New York, pp 347–363Google Scholar
  17. Gorr TA, Cahn JD, Yamagata H, Bunn HF (2004) Hypoxia-induced synthesis of hemoglobin in the crustacean Daphnia magna is hypoxia-inducible factor-dependent. J Biol Chem 279:36038–36047PubMedCrossRefGoogle Scholar
  18. Gouet P, Courcelle E, Stuart DI, Metoz F (1999) ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 15:305–308PubMedCrossRefGoogle Scholar
  19. Greenaway P (1985) Calcium balance and molting in the crustacea. Biol Rev Camb Philos Soc 60:425–454CrossRefGoogle Scholar
  20. Guadagnoli JA, Braun AA, Roberts SP, Reiber CL (2005) Environmental hypoxia influences hemoglobin subunit composition in the branchiopod crustacean Triops longicaudatus. J Exp Biol 208:3543–3551PubMedCrossRefGoogle Scholar
  21. Heisler N (1986) Buffering and transmembrane ion transfer processes. In: Heisler N (ed) Acid-base regulation in animals. Elsevier, Amsterdam, pp 3–47Google Scholar
  22. Héruoard E (1905) La circulation chez les Daphnies. Mem Soc Zool Fr 18:214–232Google Scholar
  23. Horne FR (1966) Some aspects of ionic regulation in the tadpole shrimp Triops longicaudatus. Comp Biochem Physiol 19:313–316CrossRefGoogle Scholar
  24. Horne FR (1968) Survival and ionic regulation of Triops longicaudatus in various salinities. Physiol Zool 41:180–186Google Scholar
  25. Horne FR, Beyenbach KW (1971) Physiological properties of hemoglobin in the branchiopod crustacean Triops. Am J Physiol 220:1875–1881PubMedGoogle Scholar
  26. Horne FR, Beyenbach KW (1974) Physicochemical features of hemoglobin of the crustacean, Triops longicaudatus. Arch Biochem Biophys 161:369–374PubMedCrossRefGoogle Scholar
  27. Howell BJ, Rahn H, Goodfellow D, Herreid C (1973) Acid-base regulation and temperature in selected invertebrates as a function of temperature. Am Zool 13:557–563Google Scholar
  28. Ilan E, Daniel E (1979a) Haemoglobin from the tadpole shrimp, Lepidurus apus lubbocki: Characterization of the molecule and determination of the number of polypeptide chains. Biochem J 183:325–330PubMedGoogle Scholar
  29. Ilan E, Daniel E (1979b) Structural diversity of arthropod extracellular haemoglobins. Comp Biochem Physiol B Biochem Mol Biol 63:303–308CrossRefGoogle Scholar
  30. Jensen FB, Malte H (1990) Acid-base and electrolyte regulation, and hemolymph gas transport in crayfish, Astacus astacus, exposed to soft, acid water with and without aluminum. J Comp Physiol B 160:483–490Google Scholar
  31. Kao YH, Fitch CA, Bhattacharya S, Sarkisian CJ, Lecomte JTJ, Garcia-Moreno B (2000) Salt effects on ionization equilibria of histidines in myoglobin. Biophys J 79:1637–1654PubMedCrossRefGoogle Scholar
  32. Lamkemeyer T, Paul RJ, Stöcker W, Yiallouros I, Zeis B (2005) Macromolecular isoforms of Daphnia magna haemoglobin. Biol Chem 386:1087–1096PubMedCrossRefGoogle Scholar
  33. Lamkemeyer T, Zeis B, Decker H, Jaenicke E, Waschbusch D, Gebauer W, Markl J, Meissner U, Rousselot M, Zal F, Nicholson GJ, Paul RJ (2006) Molecular mass of macromolecules and subunits and the quaternary structure of hemoglobin from the microcrustacean Daphnia magna. FEBS J 273:3393–3410PubMedCrossRefGoogle Scholar
  34. Li H, Robertson AD, Jensen JH (2005) Very fast empirical prediction and rationalization of protein pKa values. Proteins Struct Funct Bioinform 61:704–721CrossRefGoogle Scholar
  35. Lukin JA, Ho C (2004) The structure-function relationship of hemoglobin in solution at atomic resolution. Chem Rev 104:1219–1230PubMedCrossRefGoogle Scholar
  36. Matthews CM, Trotman CNA (1998) Ancient and recent intron stability in the Artemia hemoglobin gene. J Mol Evol 47:763–771PubMedCrossRefGoogle Scholar
  37. McMahon BR (2001) Control of cardiovascular function and its evolution in Crustacea. J Exp Biol 204:923–932PubMedGoogle Scholar
  38. McMahon BR, Butler PJ, Taylor EW (1978) Acid base changes during recovery from disturbance and during long term hypoxic exposure in the lobster Homarus vulgaris. J Exp Zool 205:361–370CrossRefGoogle Scholar
  39. Morgan DO, McMahon BR (1982) Acid tolerance and effects of sublethal acid exposure on iono-regulation and acid-base status in two crayfish Procambarus clarki and Orconectes rusticus. J Exp Biol 97:241–252Google Scholar
  40. Morris S, Taylor AC, Bridges CR, Grieshaber MK (1985) Respiratory properties of the hemolymph of the intertidal prawn Palaemon elegans (Rathke). J Exp Zool 233:175–186CrossRefGoogle Scholar
  41. Pirow R, Wollinger F, Paul RJ (1999) The sites of respiratory gas exchange in the planktonic crustacean Daphnia magna: An in vivo study employing blood haemoglobin as an internal oxygen probe. J Exp Biol 202:3089–3099PubMedGoogle Scholar
  42. Pirow R, Hellmann N, Weber RE (2007) Oxygen binding and its allosteric control in hemoglobin of the primitive branchiopod crustacean Triops cancriformis. FEBS J 274:3374–3391PubMedCrossRefGoogle Scholar
  43. Rahn H (1966) Aquatic gas exchange: theory. Respir Physiol 1:1–12PubMedCrossRefGoogle Scholar
  44. Risler JL, Delorme MO, Delacroix H, Henaut A (1988) Amino acid substitutions in structurally related proteins—a pattern recognition approach: determination of a new and efficient scoring matrix. J Mol Biol 204:1019–1029PubMedCrossRefGoogle Scholar
  45. Rousselot M, Jaenicke E, Lamkemeyer T, Harris JR, Pirow R (2006) Native and subunit molecular mass and quaternary structure of the hemoglobin from the primitive branchiopod crustacean Triops cancriformis. FEBS J 273:4055–4071PubMedCrossRefGoogle Scholar
  46. Sinha NP, Dejours P (1980) Ventilation and blood acid-base balance of the crayfish as functions of water oxygenation (40–1500 torr). Comp Biochem Physiol A Physiol 65:427–432CrossRefGoogle Scholar
  47. Stenderup JT, Olesen J, Glenner H (2006) Molecular phylogeny of the Branchiopoda (Crustacea)—multiple approaches suggest a ‘diplostracan’ ancestry of the Notostraca. Mol Phylogenet Evol 41:182–194PubMedCrossRefGoogle Scholar
  48. Stewart PA (1978) Independent and dependent variables of acid-base control. Respir Physiol 33:9–26PubMedCrossRefGoogle Scholar
  49. Stumm W, Morgan JJ (1995) Aquatic chemistry. Wiley, New YorkGoogle Scholar
  50. Taylor EW, Wheatly MG (1981) The effect of long-term aerial exposure on heart rate, ventilation, respiratory gas exchange and acid-base status in the crayfish Austropotamobius pallipes. J Exp Biol 92:109–124Google Scholar
  51. Terwilliger RC (1980) Structures of invertebrate hemoglobins. Am Zool 20:53–67Google Scholar
  52. Terwilliger NB (1992) Molecular structure of the extracellular heme proteins. In: Mangum CP (ed) Advances in comparative and environmental physiology: blood and tissue oxygen carriers, vol 13. Springer, Berlin, pp 193–229Google Scholar
  53. Toulmond A (1992) Properties and functions of extracellular heme proteins. In: Mangum CP (ed) Advances in comparative and environmental physiology: blood and tissue oxygen carriers, vol 13. Springer, Berlin, pp 231–256Google Scholar
  54. Truchot JP (1975) Blood acid-base changes during experimental emersion and reimmersion of the intertidal crab Carcinus maenas (L.). Respir Physiol 23:351–360PubMedCrossRefGoogle Scholar
  55. Truchot JP (1976) Carbon dioxide combining properties of the blood of the shore crab, Carcinus maenas (L.): CO2-dissociation curves and Haldane effect. J Comp Physiol 112:283–293Google Scholar
  56. Truchot JP (1987) Comparative aspects of extracellular acid-base balance. Springer, BerlinGoogle Scholar
  57. Van Beek GGM, De Bruin SH (1980) Identification of the residues involved in the oxygen-linked chloride-ion binding sites in human deoxyhemoglobin and oxyhemoglobin. Eur J Biochem 105:353–360PubMedCrossRefGoogle Scholar
  58. Vandenberg CJ, Matthews CM, Trotman CNA (2002) Variant subunit specificity in the quaternary structure of Artemia hemoglobin. Mol Biol Evol 19:1288–1291PubMedGoogle Scholar
  59. Vehstedt R (1941) Über Bau, Tätigkeit und Entwicklung des Rückengefäßes und des lakunären Systems von Artemia salina, var. arieta. Z wiss Zool 154:1–39Google Scholar
  60. Vinogradov SN (1985) The structure of invertebrate extracellular hemoglobins (erythrocruorins and chlorocruorins). Comp Biochem Physiol B Biochem Mol Biol 82:1–15CrossRefGoogle Scholar
  61. Weber RE, Hagerman L (1981) Oxygen and carbon dioxide transporting qualities of hemocyanin in the hemolymph of a natant decapod Palaemon adspersus. J Comp Physiol 145:21–27Google Scholar
  62. Weber A, Pirow R (2008) Physiological responses of Daphnia pulex to acid stress. BMC Physiol (accepted for publication)Google Scholar
  63. Weber RE, Vinogradov SN (2001) Nonvertebrate hemoglobins: functions and molecular adaptations. Physiol Rev 81:569–628PubMedGoogle Scholar
  64. Whiteley NM (1999) Acid-base regulation in crustaceans: the role of bicarbonate ions. In: Egginton S, Taylor EW, Raven JA (eds) Regulation of acid-base status in animals and plants. Cambridge University Press, CambridgeGoogle Scholar
  65. Wilkens JL (1999) Evolution of the cardiovascular system in Crustacea. Am Zool 39:199–214Google Scholar
  66. Wood CM, Rogano MS (1986) Physiological responses to acid stress in crayfish (Orconectes): hemolymph ions, acid-base status, and exchanges with the environment. Can J Fish Aquat Sci 43:1017–1026CrossRefGoogle Scholar
  67. Zeis B, Lamkemeyer T, Paul RJ, Nunes F, Schwerin S, Koch M, Schütz W, Madlung J, Fladerer C, Pirow R (2008) Acclimatory responses of the Daphnia pulex proteome to environmental changes. I. Chronic exposure to hypoxia affects the oxygen transport system and carbohydrate metabolism. BMC Physiol (accepted for publication)Google Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Ralph Pirow
    • 1
  • Ina Buchen
    • 1
  • Marc Richter
    • 1
  • Carsten Allmer
    • 1
  • Frank Nunes
    • 1
  • Andreas Günsel
    • 2
  • Wiebke Heikens
    • 2
  • Tobias Lamkemeyer
    • 3
  • Björn M. von Reumont
    • 4
  • Stefan K. Hetz
    • 5
  1. 1.Institute of ZoophysiologyUniversity of MünsterMünsterGermany
  2. 2.German Environmental Specimen Bank, Faculty of MedicineUniversity of MünsterMünsterGermany
  3. 3.Proteome Center Tübingen, Interfaculty Institute for Cell BiologyEberhard-Karls University of TübingenTübingenGermany
  4. 4.Zoologisches Forschungsmuseum Alexander KoenigBonnGermany
  5. 5.Department of Animal PhysiologyHumboldt University of BerlinBerlinGermany

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