Historical reconstructions of evolving physiological complexity: O 2 secretion in the eye and swimbladder of fishes

Journal of Experimental Biology

Volumn 210, Issue 9, 2007, Pages 1641-1652

  Berenbrink, Michael ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

Choroid; Oxygen secretion; Phylogenetic reconstruction; Rete mirabile; Root effect; Swimbladder

Indexed keywords

HEMOGLOBIN; OXYGEN;

AIR SAC; ANIMAL; COMPARATIVE STUDY; EVOLUTION; EYE; FISH; GENETICS; METABOLISM; METHODOLOGY; MOLECULAR EVOLUTION; PH; PHYLOGENY; PHYSIOLOGY; REVIEW; SECRETION; SYSTEMS BIOLOGY; VASCULARIZATION;

AIR SACS; ANIMALS; EVOLUTION; EVOLUTION, MOLECULAR; EYE; FISHES; HEMOGLOBINS; HYDROGEN-ION CONCENTRATION; OXYGEN; PHYLOGENY; SYSTEMS BIOLOGY;

PISCES; TELEOSTEI;

EID: 34249722584     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.003319     Document Type: Review

References (90)

1. Alexander, R. McN. (1966). Physical aspects of swimbladder function. Biol. Rev. 41, 141-176.
2. Berenbrink, M. (1995). Die Kontrolle des intrazellulären pH in den Erythrozyten von Knochenfischen. II. Die Bedeutung der Pseudobranchien für den Säure-Base Haushalt des Blutes und die Sauerstoffkonzentrierung im Auge von Knochenfischen. [The control of intracellular pH in erythrocytes of bony fishes. II. The role of the pseudobranchs for the acid-base status of the blood and oxygen concentrating in the eye of bony fishes]. PhD thesis, University of Düsseldorf, pp. 77-164. Aachen: Shaker Verlag.
3. Berenbrink, M. (2006). Evolution of vertebrate haemoglobins: histidine side chains, specific buffer value and Bohr effect. Respir. Physiol. Neurobiol. 154, 165-184.
4. Berenbrink, M. and Bridges, C. R. (1994). Catecholamine-activated sodium/proton exchange in red blood cells of the marine teleost Gadus morhua. J. Exp. Biol. 192, 253-267.
5. Berenbrink, M., Koldkjær, P., Kepp, O. and Cossins, A. R. (2005). Evolution of oxygen secretion in fishes and the emergence of a complex physiological system. Science 307, 1752-1757.
6. Biot, J. B. (1807). Sur la nature de l'air contenu dans la vessie natatoire des poissons. Mém. Phys. Chem. Soc. Arcueil 1, 252-281.
7. Block, B. A. and Carey, F. G. (1985). Warm brain and eye temperatures in sharks. J. Comp. Physiol. B 156, 229-236.
8. Block, B. A., Finnerty, J. R., Stewart, A. F. R. and Kidd, J. (1993). Evolution of endothermy in fish: mapping physiological traits on a molecular phytogeny. Science 260, 210-214.
9. Bohr, C. (1894). The influence of section of the vagus nerve on the disengagement of gases in the air-bladder of fishes. J. Physiol. 15, 494-499.
10. Bohr, C., Hasselbalch, K. A. and Krogh, A. (1904). Über einen in biologischer Beziehung wichtigen Einfluss, den die Kohlensäurespannung des Blutes auf dessen Sauerstoffbindung übt. Skand. Arch. Physiol. 16, 402-412.
11. Bonaventura, C., Crumblis, A. L. and Weber, R. E. (2004). New insights into the proton-dependent oxygen affinity of Root effect haemoglobins. Acta Physiol. Scand. 182, 245-258.
12. Brauner, C. J. and Berenbrink, M. (2007). Gas transport and exchange. In Primitive Fishes. Fish Physiology, vol. 27 (ed. D. J. McKenzie, A. P. Farrell and C. J. Brauner). Academic Press (in press).
13. 2 and fixed acid in the blood of the eel, Anguilla anguilla. Resp. Physiol. 51, 275-286.
14. Bridges, C. R., Berenbrink, M., Müller, R. and Waser, W. (1998). Physiology and biochemistry of the pseudobranch: an unanswered question? Comp. Biochem. Physiol. 119A, 67-77.
15. Brittain, T. (1987). The Root effect. Comp. Biochem. Physiol. 86B, 473-481.
16. Brittain, T. (2005). Root effect hemoglobins. J. Inorg. Biochem. 99, 120-129.
17. Carey, F. G. (1973). Fishes with warm bodies. Sci. Am. 228, 36-44.
18. Fahlen, G. (1959). Rete mirabile in the gas bladder of Coregonus lavaretus. Nature 184, 1001-1002.
19. Fänge, R. (1966). Physiology of the swimbladder. Physiol. Rev. 46, 299-322.
20. Farmer, M., Fyhn, H. J., Fyhn, U. E. H. and Noble, R. W. (1979). Occurrence of Root effect hemoglobins in Amazonian fishes. Comp. Biochem. Physiol. 62A, 115-124.
21. Fletcher, L. B. and Crawford, J. D. (2001). Acoustic detection by sound-producing fishes (Mormyridae): the role of gas-filled tympanic bladders. J. Exp. Biol. 204, 175-183.
22. Garland, T., Jr, Bennett, A. F. and Rezende, E. L. (2005). Phylogenetic approaches in comparative physiology. J. Exp. Biol. 208, 3015-3035.
23. Haldane, J. S. (1922). Respiration. New Haven: Yale University Press.
24. Hall, F. G. (1924). The functions of the swimbladder of fishes. Biol. Bull. 47, 79-126.
25. Harrison, R. G. and Weiner, J. S. (1949). Vascular patterns of the mammalian testis and their functional significance. J. Exp. Biol. 26, 304-316.
26. Heisler, N (1986). Comparative aspects of acid-base regulation. In Acid-Base Regulation in Animals (ed. N. Heisler), pp. 397-450. Amsterdam: Elsevier.
27. Hill, R. W., Wyse, G. A. and Anderson, M. (2004). Animal Physiology, p. 591. Sunderland, MA: Sinauer.
28. Hüfner, G. (1892). Zur physikalischen Chemie der Schwimmblasengase. Arch. Anat. Physiol., Physiol. Abth. 1892, 54-80.
29. Ito, N., Komiyama, N. H. and Fermi, G. (1995). Structure of deoxyhaemoglobin of the Antarctic fish Pagothenia bernacchii with an analysis of the structural basis of the Root effect by comparison of the liganded and unliganded haemoglobin structures. J. Mol. Biol. 250, 648-658.
30. Jacobs, W. (1930). Untersuchungen zur Physiologie der Schwimmblase der Fische. Zeitschr. Vergl. Physiol. 11, 565-629.
31. Jensen, F. B. (1989). Hydrogen-ion equilibria in fish hemoglobins. J. Exp. Biol. 143, 225-234.
32. Jessen, C. (2001). Selective brain cooling in mammals and birds. Jpn. J. Physiol. 51, 291-301.
33. Jones, F. H. R. and Marshall, N. B. (1953). The structure and functions of the teleost swimbladder. Biol. Rev. 28, 16-83.
34. Kemper, W. F., Lindstedt, S. L., Hartzler, L. K., Hicks, J. W. and Conley, K. E. (2001). Shaking up glycolysis: sustained, high lactate flux during aerobic rattling. Proc. Natl. Acad. Sci. USA 98, 723-728.
35. Kobayashi, H., Pelster, B., Piiper, J. and Scheid, P. (1989). Significance of the Bohr effect for tissue oxygenation in a model with counter-current blood flow. Resp. Physiol. 76, 277-288.
36. 2 secretion in the swimbladder of the eel. Resp. Physiol. 79, 231-242.
37. Krogh, A. (1922). The Anatomy and Physiology of the Capillaries. New Haven: Yale University Press.
38. Krogh, A. and Leitch, I. (1919). The respiratory function of the blood in fishes. J. Physiol. 52, 288-300.
39. 2-Druck. Naturwissenschaften 49, 428-429.
40. Lapennas, G. N. and Schmidt-Nielsen, K. (1977). Swimbladder permeability to oxygen. J. Exp. Biol. 67, 175-196.
41. Linthicum, D. S. and Carey, F. G. (1972). Regulation of brain and eye temperatures by the bluefin tuna. Comp. Biochem. Physiol. 43A, 425-433.
42. Lukin, J. A. and Ho, C. (2004). The structure-function relationship of hemoglobin in solution at atomic resolution. Chem. Rev. 104, 1219-1230.
43. Maddison, D. R. and Maddison, W. P. (2000). MacClade 4, analysis of phylogeny and character evolution. Version 4. Sunderland, MA: Sinauer Assoc.
44. Mazzarella, L., D'Avino, R., di Prisco, G., Savino, C., Vitagliano, L., Moody, P. C. E. and Zagari, A. (1999). Crystal structure of Trematomus newnesi haemoglobin re-opens the Root effect question. J. Mol. Biol. 287, 897-906.
45. Mazzarella, L., Bonomi, G., Lubrano, M. C., Merlino, A., Riccio, A., Vergara, A., Vitagliano, L., Verde, C. and diPrisco. G. (2006a). Minimal structural requirements for Root effect: crystal structure of the cathodic hemoglobin isolated from the Antarctic fish Trematomus newnesi. Proteins Struct. Funct. Bioinf. 62, 316-321.
46. Mazzarella, L., Vergara, A., Vitagliano, L., Merlino, A., Bonomi, G., Scala, S., Verde, C. and diPrisco, G. (2006b). High resolution crystal structure of deoxy hemoglobin from Trematomus bernacchii at different pH values: the role of histidine residues in modulating the strength of the Root effect. Proteins Struct. Fund. Bioinf. 65, 490-498.
47. Miya, M., Takeshima, H., Endo, H., Ishiguro, N. B., Inoue, J. G., Mukai, T., Satoh, T. P., Yamaguchi, M., Kawaguchi, A., Mabuchi, K. et al. (2003). Major patterns of higher teleostean phytogenies: a new perspective based on 100 complete mitochondrial DNA sequences. Mol. Phylogenet. Evol. 26, 121-138.
48. Murphy, W. J., Eizirik, E., Johnson, W. E., Zhang, Y. P., Ryder, O. A. and O'Brien, S. J. (2001). Molecular phylogenetics and the origins of placental mammals. Nature 409, 614-618.
49. Mylvaganam, S. E., Bonaventura, C., Bonaventura, J. and Getzoff, E. (1996). Structural basis for the Root effect in haemoglobin. Nature Struct. Biol. 3, 275-283.
50. Nelson, J. S. (1994). Fishes of the world. Third edition. New York: John Wiley & Sons, Inc.
51. Nikinmaa, M. (1992). Membrane-transport and control of hemoglobin-oxygen affinity in nucleated erythrocytes. Physiol. Rev. 722, 301-321.
52. Nishihara, H., Hasegawa, M. and Okada, N. (2006). Pegasoferae, an unexpected mammalian clade revealed by tracking ancient retroposon insertions. Proc. Natl. Acad. Sci. USA 103, 9929-9934.
53. Noble, R. W., Kwiatkowski, L. D., De Young, A., Davies, B. J., Haedrich, R. L., Tam, L.-T. and Riggs, A. F. (1986). Functional properties of hemoglobins from deep-sea fish: correlations with depth distribution and presence of a swimbladder. Biochim. Biophys. Acta 870, 552-563.
54. Parkhurst, L. J., Goss, D. J. and Perutz, M. F. (1983). Kinetic and equilibrium studies on the role of the b147 histidine in the Root effect and cooperativity in carp haemoglobin. Biochemistry 22, 5401-5409.
55. Pelster, B. (1995). Metabolism of the swimbladder tissue. In Biochemistry and Molecular Biology of Fishes, vol. 4 (ed. P. W. Hochachka and T. P. Mommsen), pp. 101-118. Amsterdam: Elsevier.
56. Pelster, B. (2004). pH regulation and swimbladder function in fish. Resp. Physiol. Neurobiol. 144, 179-190.
57. Pelster, B. and Randall, D. J. (1998). The physiology of the Root effect. In Fish Physiology: Fish Respiration, vol. 17 (ed. S. F. Perry and B. L. Tufts), pp. 113-140. New York: Academic Press.
58. Pelster, B. and Scheid, P. (1992). Countercurrent concentration and gas secretion in the fish swim bladder. Physiol. Zool. 65, 1-16.
59. Pelster, B. and Weber, R. E. (1990). Influence of organic phosphates on the Root effect of multiple fish haemoglobins. J. Exp. Biol. 149, 425-437.
60. Pelster, B. and Weber, R. E. (1991). The physiology of the Root effect. In Advances in Comparative and Environmental Physiology, vol. 8 (ed. R. Gilles), pp. 51-77. Berlin: Springer.
61. Perutz, M. F. and Brunori, M. (1982). Stereochemistry of cooperative effects in fish and amphibian hemoglobins. Nature 299, 421-426.
62. Piiper, J., Humphrey, H. T. and Rahn, H. (1962). Gas composition of pressurized, perfused gas pockets and the fish swim bladder. J. Appl. Physiol. 17, 275-282.
63. Randall, D. J., Burggren, W. and French, K. (2002). Eckert Animal Physiology, fifth edition, pp. 573-576. New York: W. H. Freeman.
64. + exchangers of eel (Anguilla anguilla) and rainbow trout (Oncorhynchus mykiss): a comparative study. J. Exp. Biol. 199, 415-426.
65. Root, R. W. (1931). The respiratory function of the blood of marine fishes. Biol. Bull. 61, 427-456.
66. Saitoh, K., Miya, M., Inoue, J. G., Ishiguro, N. B. and Nishida, M. (2003). Mitochondrial genomics of ostariophysan fishes: perspectives on phylogeny and biogeography. J. Mol. Evol. 56, 464-472.
67. Schmidt-Nielsen, K. (1997a). Animal Physiology, fifth edition, p. 1. Cambridge: Cambridge University Press.
68. Schmidt-Nielsen, K. (1997b). Animal Physiology, fifth edition, pp. 452-458. Cambridge: Cambridge University Press.
69. Scholander, P. F. (1954). Secretion of gases against high pressure in the swimbladder of deep sea fishes II. The rete mirabile. Biol. Bull. 107, 260-277.
70. Scholander, P. F. (1958). Counter current exchange. A principle in biology. Hvalrådets Skrifter 44, 1-24.
71. Scholander, P. F. and van Dam, L. (1954). Secretion of gases against high pressure in the swimbladder of deep sea fishes. I. Oxygen dissociation in blood. Biol. Bull. 107, 247-259.
72. Sherwood, L., Klandorf, H. and Yancey, P. H. (2005a). Animal Physiology, p. 1. Belmont, CA, USA: Thomson Brooks/Cole.
73. Sherwood, L., Klandorf, H. and Yancey, P. H. (2005b). Animal Physiology, p. 506. Belmont, CA, USA: Thomson Brooks/Cole.
74. Steen, J. B. (1963a). The physiology of the swimbladder in the eel Anguilla vulgaris. 1. The solubility of gases and the buffer capacity of the blood. Acta Physiol. Scand. 58, 124-137.
75. Steen, J. B. (1963b). The physiology of the swimbladder in the eel Anguilla vulgaris. 3. The mechanism of gas secretion. Acta Physiol. Scand. 59, 221-241.
76. Stipetic, E. (1939). Über das Gehörorgan der Mormyriden. Zeitschr. Vergl. Physiol. 26, 740-752.
77. Sundnes, G., Enns, T. and Scholander, P. F. (1958). Gas secretion in fishes lacking rete mirabile. J. Exp. Biol. 35, 671-676.
78. Venkatesh, B., Erdmann, M. V. and Brenner, S. (2001). Molecular synapomorphies resolve evolutionary relationships of extant jawed vertebrates. Proc. Natl. Acad. Sci. USA 98, 11382-11387.
79. Völkel, S. and Berenbrink, M. (2000). Sulphaemoglobin formation in fish: a comparison between the haemoglobin of the sulphide-sensitive rainbow trout (Oncorhynchus mykiss) and of the sulphide-tolerant common carp (Cyprinus carpio). J. Exp. Biol. 203, 1047-1058.
80. von Frisch, K. (1936). Über den Gehörsinn der Fische. Biol. Rev. 1936, 210-246.
81. von Ledebur, J. (1937). Beiträge zur Physiologie der Schwimmblase der Fische, V. Über die Beinflussung des Sauerstoffbindungsvermögens des Fischblutes durch Kohlensäure bei hohem Sauerstoffdruck. Zeitschr. Vergl. Physiol. 25, 156-169.
82. O2. J. Exp. Biol. 208, 4035-4047.
83. Willmer, P., Stone, G. and Johnston, I. (2005). Environmental Physiology of Animals, second edition, pp. 419-422. Malden, MA: Blackwell Science.
84. Winkler, B. S. (1981). Glycolytic and oxidative metabolism in relation to retinal function. J. Gen. Physiol. 77, 667-692.
85. Withers, P. C. (1992). Comparative Animal Physiology, pp. 754-756. Fort Worth: Saunders College Publishing.
86. Wittenberg, J. B. and Haedrich, R. L. (1974). The choroid rete mirabile of the fish eye. II. Distribution and relation to the pseudobranch and to the swimbladder rete mirabile. Biol. Bull. 146, 137-156.
87. Wittenberg, J. B. and Wittenberg, B. A. (1962). Active secretion of oxygen into the eye of fish. Nature 194, 106-107.
88. Wittenberg, J. B. and Wittenberg, B. A. (1974). The choroid rete mirabile of the fish eye. I. Oxygen secretion and structure: Comparison with the swimbladder rete mirabile. Biol. Bull. 146, 116-136.
89. Yan, H. Y. and Curtsinger, W. S. (2000). The otic gasbladder as an ancillary auditory structure in a mormyrid fish. J. Comp. Physiol. A 186, 595-602.
90. Yokoyama, T., Chong, K. T., Miyazaki, G., Morimoto, H., Shih, D. T.-B., Unzai, S., Tame, J. R. H. and Park, S.-Y. (2004). Novel mechanism of pH sensitivity in tuna hemoglobin. A structural explanation of the Root effect. J. Biol. Chem. 279, 28632-28640.