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Title: Acclimatory responses of the Daphnia pulex proteome to environmental changes. I. Chronic exposure to hypoxia affects the oxygen transport system and carbohydrate metabolism

Journal Article · · BMC Physiology
 [1];  [2];  [3];  [3];  [3];  [3];  [2];  [2];  [2];  [3]
  1. Univ. of Munster (Germany). Inst. of Zoophysiology; DOE/OSTI
  2. Univ. of Tubingen (Germany). Interfaculty Inst. for Cell Biology. Proteom Centrum Tubingen
  3. Univ. of Munster (Germany). Inst. of Zoophysiology

Background: Freshwater planktonic crustaceans of the genus Daphnia show a remarkable plasticity to cope with environmental changes in oxygen concentration and temperature. One of the key proteins of adaptive gene control in Daphnia pulex under hypoxia is hemoglobin (Hb), which increases in hemolymph concentration by an order of magnitude and shows an enhanced oxygen affinity due to changes in subunit composition. To explore the full spectrum of adaptive protein expression in response to low-oxygen conditions, two-dimensional gel electrophoresis and mass spectrometry were used to analyze the proteome composition of animals acclimated to normoxia (oxygen partial pressure [Po2]: 20 kPa) and hypoxia (Po2: 3 kPa), respectively. Results: The comparative proteome analysis showed an up-regulation of more than 50 protein spots under hypoxia. Identification of a major share of these spots revealed acclimatory changes for Hb, glycolytic enzymes (enolase), and enzymes involved in the degradation of storage and structural carbohydrates (e.g. cellubiohydrolase). Proteolytic enzymes remained constitutively expressed on a high level. Conclusion: Acclimatory adjustments of the D. pulex proteome to hypoxia included a strong induction of Hb and carbohydrate-degrading enzymes. The scenario of adaptive protein expression under environmental hypoxia can be interpreted as a process to improve oxygen transport and carbohydrate provision for the maintenance of ATP production, even during short episodes of tissue hypoxia requiring support from anaerobic metabolism.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
National Institutes of Health (NIH); USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division
Grant/Contract Number:
AC02-05CH11231; W-7405-ENG-36
OSTI ID:
1629743
Journal Information:
BMC Physiology, Journal Name: BMC Physiology Journal Issue: 1 Vol. 9; ISSN 1472-6793
Publisher:
BioMed CentralCopyright Statement
Country of Publication:
United States
Language:
English

References (92)

Reference points for comparisons of two-dimensional maps of proteins from different human cell types defined in a pH scale where isoelectric points correlate with polypeptide compositions journal January 1994
The astacin family of metalloendopeptidases journal July 1995
Multifunctional α-enolase: its role in diseases journal June 2001
Animal cellulases journal August 2001
Epipodite and fat cells as sites of hemoglobin synthesis in the branchiopod crustacean Daphnia magna journal November 1999
The state of the art in the analysis of two-dimensional gel electrophoresis images journal August 2007
A review of feeding and nutrition of herbivorous land crabs: adaptations to low quality plant diets journal February 2007
Trace nutrient deficiency in Daphnia magna cultured in standard medium for toxicity testing. Effects of the optimization of culture conditions on life history parameters of D. magna journal September 1990
Relationship between the haemoglobin concentration of Daphnia magna and the ambient oxygen concentration journal January 1982
The subunit structure of Daphnia pulex hemoglobin journal January 1980
The globin composition of Daphnia pulex hemoglobin and the comparison of the amino acid composition of invertebrate hemoglobins journal January 1990
Protease activity in gut of Daphnia magna: evidence for trypsin and chymotrypsin enzymes journal March 2004
Improved Prediction of Signal Peptides: SignalP 3.0 journal July 2004
Structures and mechanisms of glycosyl hydrolases journal September 1995
Low Genotypic Diversity in a Daphnia Pulex Population in a Biomanipulated Lake: The Lack of Vertical and Seasonal Variability journal September 2004
Copaifera spp. oleoresins impair Toxoplasma gondii infection in both human trophoblastic cells and human placental explants journal September 2020
Conserved catalytic machinery and the prediction of a common fold for several families of glycosyl hydrolases. journal July 1995
Heterogeneity and Differential Expression under Hypoxia of Two-domain Hemoglobin Chains in the Water Flea, Daphnia magna journal April 1999
Hypoxia-induced Synthesis of Hemoglobin in the Crustacean Daphnia magna Is Hypoxia-inducible Factor-dependent journal August 2004
Ancient Origin of Glycosyl Hydrolase Family 9 Cellulase Genes journal February 2005
Daphnia pulex didomain hemoglobin: structure and evolution of polymeric hemoglobins and their coding genes journal September 1999
Cellular adaptation to hypoxia: O 2 ‐sensing protein hydroxylases, hypoxia‐inducible transcription factors, and O 2 ‐regulated gene expression journal August 2002
Fluctuations in the haemoglobin content of Daphnia
  • Fox, Harold Munro; Hardcastle, Shelia M.; Dresel, Elisabeth I. B.
  • Proceedings of the Royal Society of London. Series B - Biological Sciences, Vol. 136, Issue 884, p. 388-399 https://doi.org/10.1098/rspb.1949.0032
journal October 1949
Factors influencing haemoglobin synthesis byDaphnia journal April 1953
Control of oxygen transport in the microcrustacean Daphnia: regulation of haemoglobin expression as central mechanism of adaptation to different oxygen and temperature conditions journal November 2004
A comparative study of cellulase and xylanase activity in freshwater crayfish and marine prawns journal April 2005
The digestion of cellulose and other dietary components, and pH of the gut in the amphipod Gammarus pulex (L.) journal October 1977
Implications of the three-dimensional structure of astacin for the structure and function of the astacin family of zinc-endopeptidases journal May 1993
Causes of variation in the haemoglobin content of Daphnia (Crustacea: Cladocera) in nature journal November 1954
Molecular mass of macromolecules and subunits and the quaternary structure of hemoglobin from the microcrustacean Daphnia magna journal July 2006
Temperature acclimation influences temperature-related behaviour as well as oxygen-transport physiology and biochemistry in the water flea Daphnia magna journal February 2003
Oxygen transport efficiency of multiple-component hemoglobin in Daphnia magna journal December 1994
Regulation of Mammalian O 2 Homeostasis by Hypoxia-Inducible Factor 1 journal November 1999
Nonvertebrate Hemoglobins: Functions and Molecular Adaptations journal April 2001
Crater landscape: two-dimensional oxygen gradients in the circulatory system of the microcrustacean Daphnia magna journal December 2004
Effects of hypoxia acclimation on morpho-physiological traits over three generations of Daphnia magna journal June 2005
Benefits of haemoglobin in the cladoceran crustacean Daphnia magna journal October 2001
Differential Haemoglobin Gene Expression in the Crustacean Daphnia magna Exposed to Different Oxygen Partial Pressures journal January 2003
Macromolecular isoforms of Daphnia magna haemoglobin journal January 2005
Cellulase activity in the freshwater amphipod Gammarus lacustris journal June 2000
Effect of Varying Oxygen Concentrations on the Filtering Rate of Daphnia Pulex journal July 1976
Bacterial endosymbionts in Asellus aquaticus (Isopoda) and Gammarus pulex (Amphipoda) and their contribution to digestion journal November 2003
Probability-based protein identification by searching sequence databases using mass spectrometry data journal December 1999
Reference points for comparisons of two-dimensional maps of proteins from different human cell types defined in a pH scale where isoelectric points correlate with polypeptide compositions journal January 1994
The astacin family of metalloendopeptidases journal July 1995
Multifunctional α-enolase: its role in diseases journal June 2001
Animal cellulases journal August 2001
The state of the art in the analysis of two-dimensional gel electrophoresis images journal August 2007
A review of feeding and nutrition of herbivorous land crabs: adaptations to low quality plant diets journal February 2007
A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding journal May 1976
Trace nutrient deficiency in Daphnia magna cultured in standard medium for toxicity testing. Effects of the optimization of culture conditions on life history parameters of D. magna journal September 1990
Relationship between the haemoglobin concentration of Daphnia magna and the ambient oxygen concentration journal January 1982
Oxygen binding properties of hemoglobins from Daphnia pulex (De Geer) journal January 1983
The subunit structure of Daphnia pulex hemoglobin journal January 1980
The globin composition of Daphnia pulex hemoglobin and the comparison of the amino acid composition of invertebrate hemoglobins journal January 1990
The use of biomarkers in Daphnia magna toxicity testing II. Digestive enzyme activity in Daphnia magna exposed to sublethal concentrations of cadmium, chromium and mercury journal September 1997
Structures and mechanisms of glycosyl hydrolases journal September 1995
Adaptation to oxygen deficiency: Contrasting patterns of haemoglobin synthesis in two coexisting Daphnia species journal May 1998
Molecular responses during cadmium-induced stress in Daphnia magna: Integration of differential gene expression with higher-level effects journal July 2007
Protease activity in gut of Daphnia magna: evidence for trypsin and chymotrypsin enzymes journal March 2004
Improved Prediction of Signal Peptides: SignalP 3.0 journal July 2004
Low Genotypic Diversity in a Daphnia Pulex Population in a Biomanipulated Lake: The Lack of Vertical and Seasonal Variability journal September 2004
Conserved catalytic machinery and the prediction of a common fold for several families of glycosyl hydrolases. journal July 1995
Heterogeneity and Differential Expression under Hypoxia of Two-domain Hemoglobin Chains in the Water Flea, Daphnia magna journal April 1999
Hypoxia-induced Synthesis of Hemoglobin in the Crustacean Daphnia magna Is Hypoxia-inducible Factor-dependent journal August 2004
Variation in and Oxygen-Binding Properties of Daphnia magna Hemoglobin journal September 1988
Ancient Origin of Glycosyl Hydrolase Family 9 Cellulase Genes journal February 2005
Daphnia pulex didomain hemoglobin: structure and evolution of polymeric hemoglobins and their coding genes journal September 1999
Cellular adaptation to hypoxia: O 2 ‐sensing protein hydroxylases, hypoxia‐inducible transcription factors, and O 2 ‐regulated gene expression journal August 2002
Fluctuations in the haemoglobin content of Daphnia
  • Fox, Harold Munro; Hardcastle, Shelia M.; Dresel, Elisabeth I. B.
  • Proceedings of the Royal Society of London. Series B - Biological Sciences, Vol. 136, Issue 884, p. 388-399 https://doi.org/10.1098/rspb.1949.0032
journal October 1949
Factors influencing haemoglobin synthesis byDaphnia journal April 1953
HIF-1 and human disease: one highly involved factor journal August 2000
Control of oxygen transport in the microcrustacean Daphnia: regulation of haemoglobin expression as central mechanism of adaptation to different oxygen and temperature conditions journal November 2004
A comparative study of cellulase and xylanase activity in freshwater crayfish and marine prawns journal April 2005
The digestion of cellulose and other dietary components, and pH of the gut in the amphipod Gammarus pulex (L.) journal October 1977
Implications of the three-dimensional structure of astacin for the structure and function of the astacin family of zinc-endopeptidases journal May 1993
Molecular mass of macromolecules and subunits and the quaternary structure of hemoglobin from the microcrustacean Daphnia magna journal July 2006
Food chain effects of sublethal ultraviolet radiation on subarctic Daphnia pulex – a field and laboratory study [Food chain effects of sublethal ultraviolet radiation on subarctic Daphnia pulex – a field and laboratory study] journal October 2006
Temperature acclimation influences temperature-related behaviour as well as oxygen-transport physiology and biochemistry in the water flea Daphnia magna journal February 2003
Oxygen transport efficiency of multiple-component hemoglobin in Daphnia magna journal December 1994
Regulation of Mammalian O 2 Homeostasis by Hypoxia-Inducible Factor 1 journal November 1999
Nonvertebrate Hemoglobins: Functions and Molecular Adaptations journal April 2001
Crater landscape: two-dimensional oxygen gradients in the circulatory system of the microcrustacean Daphnia magna journal December 2004
Effects of hypoxia acclimation on morpho-physiological traits over three generations of Daphnia magna journal June 2005
Benefits of haemoglobin in the cladoceran crustacean Daphnia magna journal October 2001
Protein Identification and Analysis Tools on the ExPASy Server book January 2005
Differential Haemoglobin Gene Expression in the Crustacean Daphnia magna Exposed to Different Oxygen Partial Pressures journal January 2003
Macromolecular isoforms of Daphnia magna haemoglobin journal January 2005
Cellulase activity in the freshwater amphipod Gammarus lacustris journal June 2000
Effect of Varying Oxygen Concentrations on the Filtering Rate of Daphnia Pulex journal July 1976
Cellulose digestion by freshwater microcrustacea1 journal September 1984
Bacterial endosymbionts in Asellus aquaticus (Isopoda) and Gammarus pulex (Amphipoda) and their contribution to digestion journal November 2003

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