Functional properties of hemoglobins from deep-sea fish: correlations with depth distribution and presence of a swimbladder

Noble, Robert W.; Kwiatkowski, Laura D.; Young, Alice De; Davis, Bonnie J.; Haedrich, Richard L.; Tam, Lei-Ting; Riggs, Austen

doi:10.1016/0167-4838(86)90265-7

Cited by 41 publications

(17 citation statements)

References 33 publications

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“…n50 values below unity at low pH are diagnostic of Root effect Hbs that secrete O2 into the swimbladders and retinae of fish (Pelster and Weber, 1991). Values of <1 can result from two populations of dissimilar heme groups, which could represent different isoHbs or α and β chains of the sets of Hbs (Noble et al, 1986). Obviously, the former possibility cannot explain the n<1 regions in the oxygenation curves of purified Hb II (Fig.·4).…”

Section: Cooperativitymentioning

confidence: 82%

Hemoglobin function in deep-sea and hydrothermal-vent endemic fish:Symenchelis parasitica(Anguillidae) andThermarces cerberus(Zoarcidae)

Weber

Hourdez

Knowles

et al. 2003

Journal of Experimental Biology

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Deep-sea hydrothermal vents probably provide the harshest physico-chemical conditions confronting metazoan animals in nature. Given the absence of information on hemoglobin (Hb) function in hydrothermal-vent vertebrates, and the complex molecular and functional adaptations observed in hydrothermal-vent invertebrates, we investigated the oxygenation reactions of Hbs from the vent-endemic zoarcid Thermarces cerberus and the deep-sea anguillid Symenchelis parasitica from adjacent habitats.Electrophoretically cathodic and anodic isoHbs from S. parasitica exhibit radical differences in O2 affinity and pH and organic phosphate (ATP) sensitivities, reflecting a division of labor as in other 'class II' fish that express both Hb types. Remarkably, the cathodic Hb (I) lacks chloride sensitivity, and the anodic Hb (II) shows anticooperativity near half-saturation at low temperature. T. cerberus isoHbs exhibit similar affinities and pH sensitivities ('class I' pattern) but much higher O2 affinities than those observed in Hbs of the temperate, shallow-water zoarcid Zoarces viviparus, which, unless compensated, reveals markedly higher blood O2 affinities in the former species. The temperature sensitivity of O2 binding to T. cerberus Hbs and the anodic S. parasitica Hb, which have normal Bohr effects, is decreased by endothermic proton dissociation, which reduces the effects of ambient temperature variations on O2 affinity. In the cathodic S. parasitica Hb, similar reduction appears to be associated with endothermic conformational changes that accompany the oxygenation reaction.

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Section: Cooperativitymentioning

confidence: 82%

Hemoglobin function in deep-sea and hydrothermal-vent endemic fish:Symenchelis parasitica(Anguillidae) andThermarces cerberus(Zoarcidae)

Weber

Hourdez

Knowles

et al. 2003

Journal of Experimental Biology

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“…The quaternary transition to R state occurs when the ␣ 1 ␤ 1 and ␣ 2 ␤ 2 dimers have at least one ligated subunit, impairing stability of the ␣ 1 ␤ 2 interface in the T state. In contrast, in Root-effect Hbs, which bind oxygen noncooperatively at lower pH values, the interface remains stable upon oxygenation in the T state, where a large subunit functional heterogeneity is observed (46,47), although its structural basis has not been established unequivocally (43). In cases where cooperativity is impaired also at alkaline or neutral pH, such as the Gadidae, Anguilla anguilla (48) and Chelidonichthys kumu, subunit heterogeneity is probably more marked (47).…”

Section: Zoarcoid Perciformsmentioning

confidence: 90%

The Oxygen Transport System in Three Species of the Boreal Fish Family Gadidae

Verde

Balestrieri

Pascale

et al. 2006

Journal of Biological Chemistry

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The Arctic and Antarctic marine faunas differ by age and isolation. Fishes of the two polar regions have undergone different regional histories that have driven the physiological diversities. Antarctic fish are highly stenothermal, in keeping with stable water temperatures, whereas Arctic fish, being exposed to seasonal temperature variations, exhibit higher physiological plasticity. This study reports the characterization of the oxygen transport system of three Arctic species of the family Gadidae, namely the Arctic cod Arctogadus glacialis, the polar cod Boreogadus saida, and the Atlantic cod Gadus morhua. Unlike Antarctic notothenioids, the blood displays high multiplicity, i.e. it has three hemoglobins, similar to many other acanthomorph teleosts. In the most abundant hemoglobin, oxygen binding is modulated by heterotropic effectors, with marked Bohr and Root effects. Remarkably, in two species (A. glacialis and B. saida), the Hill coefficient is very close to one in the whole pH range, indicating the apparent absence of cooperativity. The amino acid sequences have been used to gain insight into the evolution history of globins of polar fish. The results indicate that Arctic and Antarctic globins have different phylogenies and lead us to suggest that the selective pressure of environment stability allows the phylogenetic signal to be maintained in the Antarctic sequences, whereas environmental variability would tend to disrupt this signal in the Gadidae sequences.The main differences between the Arctic and the Antarctic are the older age and longer isolation of the latter (1). The Antarctic has been isolated and cold longer than the Arctic, with ice-sheet development preceding that in the Arctic by at least 10 million years. In a recent review, Eastman (2) wrote the following. "The Antarctic experienced a slow and discontinuous transition from a warm-water system in the early Tertiary (15°C) to the cold-water system of today (Ϫ1.87°C). The first glaciation, including shelf-ice formation, had occurred 36 million years ago (mya) 2 in the early Oligocene. About 25 mya, the formation of the Polar Front, which followed the opening of the Drake passage, further isolated the Antarctic marine fauna from the world ocean. Although Europe began to separate from Greenland in the late Cretaceous, the exchange of Atlantic and Arctic waters through the passage between Greenland and the Svalbard islands was not possible until 27 mya. The Arctic region was in a high latitude position by the early Tertiary, but the climate remained temperate with water temperatures of 10 -15°C. Arctic land masses reached their present positions, and temperatures dropped below freezing during the Miocene about 10 -15 mya."The Antarctic and Arctic fish faunas differ in age, endemism (denoting species native to a given geographical area), and taxonomic diversity. In the southern ocean, the fauna includes 322 species grouped in 50 families (3), whereas the Arctic fauna has 416 species of 96 families. In the Antarctic, endemism reaches 88% and ris...

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“…5, the markedly low co-operativity of oxygen binding in the whole pH range and under all experimental conditions examined, with the Hill coefficient in the range 1.0-0.85 (being higher than 1 .O only at pH > 7.5), finds an explanation. The value of h,,, < 1 at pH < 7.0 can be accounted for by a pH-dependent stabilisation of the T state, accompanied by a marked subunit functional heterogeneity within the tetramer, a feature already found in other Root-effect fish hemoglobins (Noble et a]., 1970(Noble et a]., , 1986Brunori et al, 1978;Pennelly et al, 1978;Galdames-Portus et al, 1979;Morris and Gibson, 1982; Prisco et al, 1988). However, a rise in pH brings about the appearance in oxygenated hemoglobin of a predominance of the R state, as indicated by the autocatalytic shape of the oxygen-dissociation curve (see curve a in Fig.…”

Section: Functional Propertiesmentioning

confidence: 99%

A polymerising Root‐effect fish hemoglobin with high subunit heterogeneity

Fago¹,

Romano²,

Tamburrini³

et al. 1993

European Journal of Biochemistry

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The blood of the teleost Chelodunichthys kumu, living in the temperate waters of New Zealand, contains a single hemoglobin. The complete amino acid sequence of the a and / 3 chain has been established. The presence of a reactive Cys in the external position /3CD8(49) causes polymerisation through intermolecular disulfide bridges between p chains, with no alteration of functional features.C. kumu Root-effect hemoglobin displays very low or no subunit co-operativity in the physiological pH range. Kinetic experiments on the oxygen dissociation and binding of carbon monoxide show a marked, pH-dependent functional heterogeneity of the two chains, which contributes to the observed reduction of co-operativity. In contrast, kinetic heterogeneity was not observed in the process of CO dissociation, indicating that functional differences between the subunits are detectable only for the dynamic ligand association pathway. The allosteric effector, ATP, seems to increase the pK, of the proton-linked effect on the slow-reacting subunit, affecting the quaternary equilibrium through stabilisation of the T state at lower pH, rather than enhancing the functional heterogeneity itself. In position Ell of both chains, Val (usually present at the distal side of the heme), is substituted by Ile. Although this residue has been shown not to significantly alter ligand binding to the a chain, to some extent it can perturb the access of oxygen to the p chain. Thus, this substitution may be the main reason for subunit functional heterogeneity.The study of fish hemoglobins over the past years has revealed a wide range of different structural and functional properties, often associated with the multiplicity of components present in individual animals. Consequently, the regulation of oxygen binding on a structural basis cannot be interpreted generally and oxygen binding of individual hemoglobins may be the result of different molecular interactions.In several fish hemoglobins, a large reduction in the oxygen affinity and co-operativity is observed at low pH values (and in the presence of allosteric effectors), so that these hemoglobins cannot be fully saturated even with pure oxygen at pressures of several Pascalles (Scholander and Van Dam, 1954;Brunori et al., 1978). According to the interpretation of this effect (called the Root effect) in the framework of the two-state model of Monod et al. (1965), the T-R equilibrium is shifted by protons and/or other allosteric effectors towards the low-affinity conformation, thereby inhibiting the ligandlinked quaternary transitions and abolishing the co-operativity. Under these conditions, the Hill coefficient may drop to values d 1 .O, if associated to a subunit functional heterogeneity. A stereochemical interpretation of the Root effect was proposed by Perutz and Brunori (1982), who suggested that a few residues of the chain might be responsible for a relative stabilisation of the T state with respect to the R state. Although some Hb A mutants (Nagai et al., 1985;Luisi and Nagai, 1986) and Antarctic fi...

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Functional properties of hemoglobins from deep-sea fish: correlations with depth distribution and presence of a swimbladder

Cited by 41 publications

References 33 publications

Hemoglobin function in deep-sea and hydrothermal-vent endemic fish:Symenchelis parasitica(Anguillidae) andThermarces cerberus(Zoarcidae)

Hemoglobin function in deep-sea and hydrothermal-vent endemic fish:Symenchelis parasitica(Anguillidae) andThermarces cerberus(Zoarcidae)

The Oxygen Transport System in Three Species of the Boreal Fish Family Gadidae

A polymerising Root‐effect fish hemoglobin with high subunit heterogeneity

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