Skip to main content
Log in

Effects of Environmental Contaminants on Hemoglobin Gene Expression in Daphnia magna: A Potential Biomarker for Freshwater Quality Monitoring

  • Published:
Archives of Environmental Contamination and Toxicology Aims and scope Submit manuscript

Abstract

Daphnia hemoglobin (Hb) is one of the widely investigated invertebrate respiratory pigment. In this study, alteration of Daphnia magna Hb was evaluated in terms of its gene expression, using four D. magna Hb open reading frames (ORFs), by exposure of various chemicals, such as nonylphenol (NP), bisphenol A (BPA), benzo[a]pyrene (B[a]P), chloropyriphos (CP), paraquat dichloride (PQ), and lead nitrate (Pb), under laboratory conditions. A Daphnia reproduction test was also conducted to test the ecotoxicological relevance of chemical-induced Daphnia Hb gene expression. Daphnia Hb gene expression increased by most of tested chemicals. Nonylphenol induced all four Hb ORFs, and an increase in D. magna hemoglobin 2 (dmhb2), dmhb3, and dmhb4 gene expression was exposure concentration dependent. Although BPA and B[a]P also induced most of the Hb genes, the degree of increase was less than two-fold compared to the control. For CP and Pb exposure, an increase in dmhb2 and dmhb4 gene expression was the most significant among the four Daphnia Hb ORFs. Each ORF might exhibit different sensitivities to chemical stress; of the four ORFs studied, an increase in dmhb2 and dmhb4 gene expression was the most significant. It seems clear that Daphnia Hb has a considerable potential as a biomarker for freshwater toxicity monitoring, as an increase in Hb gene expression seems to be correlated with a decrease in reproduction in this animal. The results suggest that Daphnia Hb could give useful information to diagnose general health conditions in a freshwater ecosystem. Considering the potential of D. magna as a biomonitoring species and the physiological particularities of its respiratory pigments, Daphnia Hb could be developed as a biomarker for ecotoxicity monitoring.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Caquet T, Lagadic L (2000) Consequences of individual-level alterations on population dynamics and community structure and function. In: Lagadic L, Caquet T, Amiard JC, Ramade F (eds) Use of biomarkers for environmental quality assessment. Science Publishers, Enfield, UK, pp 79–111

    Google Scholar 

  • Depledge MH, Amaral-Mendes JJ, Daniel B, et al. (1993) The conceptual basis of the biomarker approach. In: Peakall DG, Shugart LR (eds) Biomarkers: Research and application in the assessment of environmental health. Springer-Verlag, Berlin, pp 15–29

    Google Scholar 

  • Depledge MH, Fossi MC (1994) The role of biomarkers in environmental assessment (2). Invertebrates. Ecotoxicology 3:161–172

    Article  Google Scholar 

  • Fox HM (1955) The effect of oxygen on the concentration of haem in invertebrates. Proc R Soc B 143:203–214

    Article  CAS  Google Scholar 

  • Gorr TA, Cahn JD, Yamagata H, Bunn HF (2004) Hypoxia induced synthesis of hemoglobin in the crustacean Daphnia magna is HIF dependent. J Biol Chem 279:36,038–36,047

    Google Scholar 

  • Gorr TA, Rider CV, Wang HY, Olmstead AW, LeBlanc GA (2006) A candidate juvenoid hormone receptor cis-element in the Daphnia magna hb2 hemoglobin gene promoter. Mol Cell Endocrinol 247:91–102

    Article  CAS  Google Scholar 

  • Hebert PDN, Um YM, Prokopowich CD, Taylor DJ (1999) Gene conversion and evolution of daphniid hemoglobins (Crustacea, Cladocera). J Mol Evol 49:769–779

    Article  CAS  Google Scholar 

  • Hyne RV, Maher WA (2003) Invertebrate biomarkers: links to toxicosis that predict population decline. Ecotoxicol Environ Safety 54:366–374

    Article  CAS  Google Scholar 

  • Kimura S, Tokishita S, Ohta T, Kobayashi M (1999) Heterogeneity and differential expression under hypoxia of two-domain hemoglobin chains in the water flea, Daphnia magna. J Biol Chem 274:10,649–10,653

    Google Scholar 

  • Kobayashi M, Hoshi T (1982) Relationship between the haemoglobin concentration of Daphnia magna and the ambient oxygen concentration. Comp Biochem Physiol 72A:247–249

    Article  CAS  Google Scholar 

  • Lankester ER (1871) Ü ber das Vorkommen von Haemoglobin in den Muskeln der Mollusken und die Verbreitung desselben in den lebendigen Organismen. Pflügers Arch Ges Physiol 4:315–320

    Article  Google Scholar 

  • Lee SM, Lee SB, Park CH, Choi J (2006) Expression of heat shock protein and hemoglobin genes in Chironomus tentans (Diptera, Chironomide) larvae exposed to various environmental pollutants: a potential biomarker of freshwater monitoring. Chemosphere 65:1074–1081

    Article  CAS  Google Scholar 

  • OECD (1984) Guidelines for testing of chemicals, Vol. 1, Section 2: Effects on biotic systems, Daphnia magna acute immobilization Test 202. OECD, Paris

  • Osmulski PA, Leyko W (1986) Structure, function and physiological role of Chironomus haemoglobin. Comp Biochem Physiol B: Biochem 85:701–722

    Article  Google Scholar 

  • Pane EF, Smith C, McGeer JC, Wood CM (2003) Mechanisms of acute and chronic waterborne nickel toxicity in the freshwater cladoceran, Daphnia magna. Environ Sci Technol 37:4382–4389

    Article  CAS  Google Scholar 

  • Paul RJ, Zeis B, Lamkemeyer T, Seidl M, Pirow R (2004) Control of oxygen transport in the microcrustacean Daphnia: regulation of haemoglobin expression as central mechanism of adaptation to different oxygen and temperature conditions. Acta Physiol Scand 182:259–275

    Article  CAS  Google Scholar 

  • Prosser CL, Brown FA (1961) Comparative animal physiology. Saunders, Philadelphia

    Google Scholar 

  • Rider CV, Gorr TA, Olmstead AW, Wasilak BA, LeBlanc GA (2005) Stress signaling: coregulation of hemoglobin and male sex determination through a terpenoid signaling pathway in a crustacean. J Exp Biol 208:15–23

    Article  CAS  Google Scholar 

  • Rider CV, LeBlanc GA (2006) Atrazine stimulates hemoglobin accumulation in Daphnia magna: Is it hormonal or hypoxic? Toxicol Sci 93:443–449

    Article  CAS  Google Scholar 

  • Rotchell JM, Ostrander GK (2003) Molecular markers of endocrine disruption in aquatic organisms. J Toxicol Environ Health B 6:453–496

    Article  CAS  Google Scholar 

  • Terwilliger RC (1980) Structure of invertebrate hemoglobins. Am Zool 20:53–67

    CAS  Google Scholar 

  • Terwilliger NB (1998) Functional adaptations of oxygen-transport proteins. J Exp Biol 201:1085–1098

    CAS  Google Scholar 

  • Tokishita S, Shiga Y, Kimura S (1997) Cloning and analysis of a cDNA encoding a two-domain hemoglobin chain from the water flea Daphnia magna. Gene 189:73–78

    Article  CAS  Google Scholar 

  • Vinogradov SN (1985) The structure of invertebrate extracellular hemoglobins (erythrocruorins and chlorocruorins). Comp Biochem Physiol 82B:1–15

    CAS  Google Scholar 

  • Weber RE (1980) Functions of invertebrate hemoglobins with special reference to adaptations to environmental hypoxia. Am Zool 20:79–101

    CAS  Google Scholar 

  • Weber RE, Vinogradov SN (2001) Nonvertebrate hemoglobins: functions and molecular adaptations. Physiol Rev 81:569–628

    CAS  Google Scholar 

  • Yoshimi T, Minowa K, Karouna-Renier NK, Watanabe C, Sugay AY, Miura T (2002) Activation of a stress-induced gene by insecticides in the midge Chironomus yoshimatsui. J Biochem Mol Toxicol 16:10–17

    Article  CAS  Google Scholar 

  • Zeis B, Becher B, Goldmann T, et al. (2003b) Differential haemoglobin gene expression in the crustacean Daphnia magna exposed to different oxygen partial pressures. Biol Chem 384:1133–1145

    Google Scholar 

  • Zeis B, Becher B, Lamkemeyer T, Rolf S, Pirow R, Paul RJ (2003a) The process of hypoxic induction of Daphnia magna hemoglobin: subunit composition and functional properties. Comp Biochem Physiol B: Biochem Mol Biol 143:243–252

    Google Scholar 

Download references

Acknowledgment

This work was supported by the Korean Ministry of Environment through the Ecotechnopia 21 project.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jinhee Choi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ha, MH., Choi, J. Effects of Environmental Contaminants on Hemoglobin Gene Expression in Daphnia magna: A Potential Biomarker for Freshwater Quality Monitoring. Arch Environ Contam Toxicol 57, 330–337 (2009). https://doi.org/10.1007/s00244-007-9079-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00244-007-9079-0

Keywords

Navigation