Relationship between the haemoglobin concentration of Daphnia magna and the ambient oxygen concentration

doi:10.1016/0300-9629(82)90040-8

Comparative Biochemistry and Physiology Part A: Physiology

Volume 72, Issue 1, 1982, Pages 247-249

Comparative Biochemi...

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Abstract

1.
1. The haemoglobin (Hb) concentration of Daphnia magna was in inverse proportion to the oxygen (O₂) concentration of its environmental water. A very slight O₂decrease below air saturation induced Hb production.
2.
2. The ability of an animal to extract O₂ from environmental water with a low O₂ level depended on its Hb concentration. Even a pale animal was able to maintain constant O₂ consumption rate until the ambient O₂ concentration fell to about 20% air saturation.
3.
3. These results suggested that Hb functions only in a low O₂ concentration but that the Hb concentration was regulated over a wide range of O₂ concentration.

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Cited by (62)

Bioaccumulation and morphological traits in a multi-generation test with two Daphnia species exposed to lead
2019, Chemosphere
Citation Excerpt :
Highlighting that the oxygen levels were within the limits recommended by OECD (2012) (>3 mg/L). Haemoglobins facilitate oxygen transportation and, in a hypoxic environment, haemoglobin production tend to increase (Kobayashi and Hoshi, 1982). However, besides haemoglobin regulation by oxygen concentrations, it might also be regulated by chemical stress (Ha and Choi, 2009), being haemoglobin and stress positively correlated (Schwerin et al., 2010).
Anthropic pressure negatively affects natural environments. Lead (Pb) is a non-essential highly toxic metal that is present in aquatic ecosystems. Two daphnid species from two different latitudes, the temperate Daphnia magna and the tropical Daphnia similis were used as test-organisms to evaluate a long-term Pb exposure. Both species were exposed for nine generations to a chronic concentration of Pb (50 μg/L) and the effects were explored, considering some endpoints not commonly used in toxicity tests: body burden of Pb and presence of granules in the dorsal region of neonates, hemoglobin contents, carapace deformation and morphology, production of males and ephippia (or dormant haploid egg), changes in the eggs' colour and eggs abortion. This multi-generation test was conducted under two food regimes, the usual (3 × 10⁵ cells/mL) and the restricted (1.5 × 10⁵ cells/mL) regime. On generation F6, Pb acclimated neonates were changed to a clean media for three generations, to evaluate exposure retrieval (recovery period). Negative and adverse effects occurred through generations, but no disparity was shown between D. magna and D. similis. The D. magna Pb accumulation showed different patterns regarding food regime. Bioaccumulation was faster under usual food, rapidly reaching a saturation point, whereas a gradual increase occurred under food restriction. A successful retrieval happened regarding Pb in D. magna, since no difference between control and recovering organisms was evidenced regarding their Pb body burdens. Generational Pb exposure led to carapace malformations, Pb aggregation in neonates' dorsal region, reddish extremities, production of males, ephippia (or dormant haploid egg), and aborted eggs, and changes in the eggs’ colour (green and white). Food restriction also induced the production of males. Reddish extremities disappeared in recovering organisms and ephippia (or dormant haploid egg) did not occurred during the recovery period. Existent males revealed a shorter lifespan than females (under stress). D. magna and D. similis presented similar responses, for the endpoints analysed; however, it does not mean that this lack of sensitivity difference will be observed when other endpoints (e.g. survival, reproduction) are considered. Bioaccumulation of Pb and adverse effects occurred at the tested concentration of 50μg/L, although higher Pb levels are allowed in the environment as safe concentrations, as reported by the Brazilian legislation and the literature where effects are evidences above 400 μg/L of Pb. Pb effects on reproduction, respiration, malformation, and other adverse effects suggest that a chronic generational exposure can be harmful to both D. magna and D. similis, and that such chronic contaminated environments should not be disregarded when it comes to environmental monitoring.
Hypoxia-inducible haemoglobins of Daphnia pulex and their role in the response to acute and chronic temperature increase
2013, Biochimica et Biophysica Acta - Proteins and Proteomics
Citation Excerpt :
Eleven types of extracellular di-domain haemoglobins are present in the D. pulex genome; eight of these are part of a tandem repeat cluster [6]. A hypoxia-induced increase of Hb concentration has been described for Daphnia magna [7,8] and D. pulex [9]. For D. magna, the differential induction of multiple isoforms [10] was assigned to the presence of hypoxia-responsive elements (HRE) binding the hetero-dimeric transcription factor HIF (hypoxia-inducible factor) in the promoter regions of Hb genes [11].
Daphnia pulex is challenged by severe oxygen and temperature changes in its habitat. In response to hypoxia, the equipment of oxygen transport proteins is adjusted in quantity and quality by differential expression of haemoglobin isoforms. This study focuses on the response of 20 °C acclimated animals to elevated temperature using transcriptomic and proteomic approaches. Acute temperature stress (30 °C) induced the hypoxia-inducible Hb isoforms most strongly, resulting in an increase of the haemoglobin mRNA pool by 70% within 8 h. Long-term-acclimation to moderately elevated temperature (24 °C) only evoked minor changes of the Hb mRNA suite. Nevertheless, the concentration of the hemolymph pool of haemoglobin was elevated by 80%. In this case, the constitutive Hb isoforms showed the strongest increase, with Hb01 and Hb02 contributing by 64% to the total amount of respiratory protein. The regulation patterns upon acute temperature stress likely reflect temperature-induced tissue hypoxia, whereas in case of persisting exposure to moderately elevated temperature, acclimation processes enabled the successful return to oxygen homeostasis. This article is part of a Special Issue entitled: Oxygen Binding and Sensing Proteins.
Adaptive haemoglobin gene control in Daphnia pulex at different oxygen and temperature conditions
2011, Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology
Citation Excerpt :
Changes in P50 with measuring temperature (∆P50 ∆T−1, calculated between 10 °C and 24 °C) were considerably higher in normoxia-acclimated animals (0.071–0.080 kPa °C−1) than in hypoxia-acclimated ones (0.011–0.015 kPa °C−1). Daphnids increase haemolymph Hb concentration and Hb oxygen affinity in response to hypoxia (e.g. Fox et al., 1949; Kobayashi and Hoshi, 1982; Kobayashi et al., 1988). As a result of hypoxia-acclimation, D. pulex increased Hb concentration by a factor of maximally 14.3 (Fig. 4; 20 °C acclimation) and Hb oxygen affinity by a factor of maximally 14.8 (Fig. 5; 20 °C acclimation and 10 °C measuring temperature).
Hypoxia-induced haemoglobin (Hb) expression is a central regulatory mechanism in Daphnia in response to environmental hypoxia or warm temperatures. Changes in Hb concentration as well as Hb subunit composition, which modulate Hb oxygen affinity, guarantee the oxygen supply of tissues under these environmental conditions. Based on the sequenced D. pulex genome, Hb genes were related to the properties of haemolymph Hb, which included its concentration and oxygen affinity (both measured by spectrophotometry) as well as the Hb subunit composition (determined by 2-D gel electrophoresis and ESI-MS analysis). Permanent cultures of D. pulex acclimated to different oxygen conditions (normoxia and hypoxia) and temperatures (10 °C, 20 °C, and 24 °C), showed characteristic changes in Hb concentration, subunit composition and oxygen affinity. Several subunits (Hb4, Hb7, Hb8, and Hb10) were obviously responsible for changes in oxygen affinity including those, which carry a number of hypoxia-responsive elements (HREs) upstream of the respective gene (hb4 and hb10). Analysing the effects of different oxygen- or temperature-acclimations on Hb subunit expression in D. pulex and D. magna on a common basis (Hb concentration or oxygen affinity) revealed a general pattern of oxygen and temperature effects on Hb, which implies that Hb quantity and quality are mostly influenced by the degree of tissue hypoxia. Differences between both species in the onset of hypoxia-induced differential Hb expression and Hb oxygen affinity, which are probably related to different HRE patterns and functionally important differences in the amino acid sequence of only a few subunits, cause a reduced ability of D. pulex to adjust Hb function to temperature changes in comparison to D. magna.
Sensing and responding to hypoxia via HIF in model invertebrates
2006, Journal of Insect Physiology
Citation Excerpt :
As expected, late-stage embryos and larvae of Drosophila withstand even day-long exposures of lack of oxygen (Wingrove and O’Farrell, 1999). Despite this tolerance, adult daphnids (Kobayashi and Hoshi, 1982; Paul et al., 1997) and drosophilids (Csik, 1939; Chadwick and Gilmour, 1940) display oxyregulation in O2-uptake or behavior as long as ambient pO2 levels are non-limiting to sustain oxidative metabolism. Commonplace occurrence of oxygen independent respiratory rates amongst crustaceans (Childress, 1975; McMahon, 2001) or insects (Keister and Buck, 1974; Loudon, 1988; Hoback and Stanley, 2001) is, thus, faithfully reflected by waterflea and fruitfly models.
This past decade has brought considerable progress towards elucidating the molecular mechanisms of oxygen sensing pathways by which mammalian cells are able to detect and adjust, or succumb, to hypoxia. In contrast, far less is known about the protein and DNA constituents that endow many invertebrate species to withstand and recover from even more severe and prolonged O₂ limitations. In spite of these differences in hypoxia tolerance, inadequacy in oxygen supply is, from mammals to insects to nematodes, signaled onto the DNA level predominantly by hypoxia-inducible factors (HIFs). Across the animal kingdom, HIF accumulates in hypoxic, but not normoxic, cells and functions in a remarkably conserved pathway. Using crustacean (Daphnia magna) and insect (Drosophila melanogaster) models, work by us and others has implicated HIF in restoring O₂ delivery via stimulated hemoglobin synthesis (Daphnia) or tracheal remodeling (Drosophila). HIF is essential for these arthropods to adapt and survive during moderate O₂ limitations. A similar life-preserving role for HIF-signaling in hypoxic, but not anoxic, environments had previously been established for another stress-tolerant invertebrate model, the nematode Caenorhabditis elegans. Exploring regulations of oxygen-dependent Daphnia and Drosophila genes in cell culture and in vivo have furthermore aided in uncovering novel HIF-targeting mechanisms that might operate to fine-tune the activity of this transcription factor under steadily hypoxic, rather than changing, oxygen tensions. We conclude our review with yet another addition to the growing list of HIF's many functions: the control of cellular growth during fly development.
Hemoglobin in Arthropods—Daphnia as a Model
2020, Subcellular Biochemistry
The combined effects of hypoxia and fish kairomones on several physiological and life history traits of Daphnia
2019, Freshwater Biology

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Comparative Biochemistry and Physiology Part A: Physiology

Abstract

References (18)

Causes of variation in the haemoglobin content of Daphnia (Crustacea:CIadocera) in nature

The oxygen affinities of certain invertebrate haemoglobin

J. exp. Biol.

Fluctuations in the haemoglobin content of Daphnia

Functions of haemoglobin in Daphnia

Factors influencing haemoglobin synthesis by Daphnia

Studies on a population of Daphnia magma

J. Anim. Ecol.

The filtering rate and respiration rates of Daphnia magna and Daphnia gendali

Limnol. Oceanogr.

Studies on physiology and ecology of plankton, XXVII. O₂-consumption. thoracic limb movement and O₂-dissociation from haemoglobin of Daphnia magna in vivo

Science Rep. Niigata Univ. Ser D

Studies on physiology and ecology of plankton, XXV. Iron-content and millimolar extinction coefficient of the Daphnia haemoglobin

Science Rep. Niigata Univ. Ser. D

Cited by (62)

Bioaccumulation and morphological traits in a multi-generation test with two Daphnia species exposed to lead

Hypoxia-inducible haemoglobins of Daphnia pulex and their role in the response to acute and chronic temperature increase

Adaptive haemoglobin gene control in Daphnia pulex at different oxygen and temperature conditions

Sensing and responding to hypoxia via HIF in model invertebrates

Hemoglobin in Arthropods—Daphnia as a Model

The combined effects of hypoxia and fish kairomones on several physiological and life history traits of Daphnia

Relationship between the haemoglobin concentration of Daphnia magna and the ambient oxygen concentration

Abstract

Causes of variation in the haemoglobin content of Daphnia (Crustacea:CIadocera) in nature

The oxygen affinities of certain invertebrate haemoglobin

J. exp. Biol.

Fluctuations in the haemoglobin content of Daphnia

Functions of haemoglobin in Daphnia

Factors influencing haemoglobin synthesis by Daphnia

Studies on a population of Daphnia magma

J. Anim. Ecol.

The filtering rate and respiration rates of Daphnia magna and Daphnia gendali

Limnol. Oceanogr.

Studies on physiology and ecology of plankton, XXVII. O2-consumption. thoracic limb movement and O2-dissociation from haemoglobin of Daphnia magna in vivo

Science Rep. Niigata Univ. Ser D

Studies on physiology and ecology of plankton, XXV. Iron-content and millimolar extinction coefficient of the Daphnia haemoglobin

Science Rep. Niigata Univ. Ser. D

Studies on physiology and ecology of plankton, XXVII. O₂-consumption. thoracic limb movement and O₂-dissociation from haemoglobin of Daphnia magna in vivo