Skip to main content

Advertisement

SpringerLink
Log in

Stress Proteins (hsp70, hsp60) Induced in Isopods and Nematodes by Field Exposure to Metals in a Gradient near Avonmouth, UK

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

Heat shock proteins (hsps) are potential biomarkers for monitoring environmental pollution. In this study, the use of hsps as biomarkers in field bioassays was evaluated in terrestrial invertebrates exposed to a metal gradient near Avonmouth, UK. We investigated the hsp70 response in resident and transplanted isopods of the species Oniscus asellus and Porcellio scaber and the hsp60 response in transplanted nematodes of the species Plectus acuminatusin six field sites along the metal gradient. Considerable differences were detected in the stress responses between nematodes and isopods (isopods responded in a gradient-specific manner, nematodes did not), the two isopod species and the transplanted and resident specimens of each isopod species in the sites closest to the smelter, O. asellus residents showed high hsp70 levels while O. asellus transplanted from an unpolluted site displayed comparatively low hsp70 levels. For P. scaber, it was just the opposite. In resident isopod populations of both species, tolerant phenotypes were revealed in the most contaminated field sites. The hsp70 level in both isopod species was a suitable biomarker of effect (but of exposure only in non-tolerant individuals) even in long-term metal-contaminated field sites. The hsp60 response in the nematode alone was not a suitable biomarker for heavily contaminated soils. However, it had indicative value when related to the hsp70 response in the isopods and could be a suitable biomarker for less heavily contaminated soils.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • C.F.C. Bonting B.M.F. Willemsen W. Akkermans-Van Vliet P.J.M. Bouvet G.J.J. Koristee A.J.B. Zehnder (1992) ArticleTitleAdditional characteristics of the polyphosphate-accumulating Acinetobacter strain 210A and its identification as Acinetobacter johnsonii FEMS Microbiol. Ecol. 102 57–64 Occurrence Handle1:CAS:528:DyaK3sXns1yjsA%3D%3D

    CAS  Google Scholar 

  • M.M. Bradford (1976) ArticleTitleA rapid and sensitive method for the quantification of microgram quantitites of protein utilizing the principle of protein-dye binding Anal. Biochem. 72 248–54 Occurrence Handle10.1006/abio.1976.9999 Occurrence Handle1:CAS:528:DyaE28XksVehtrY%3D Occurrence Handle942051

    Article  CAS  PubMed  Google Scholar 

  • H.-L. Chiang S.R. Terlecky C.P. Plant J.F. Dice (1989) ArticleTitleA role for a 70-kilodalton heat shock protein in lysosomal degradation of intracellular proteins Science 246 382–5 Occurrence Handle2799391 Occurrence Handle1:CAS:528:DyaK3cXivFei

    PubMed  CAS  Google Scholar 

  • R. Dallinger P.S. Rainbow (1993) Ecotoxicology of Metals in Invertebrates. Lewis, Chelsea Michigan, USA

    Google Scholar 

  • J.M. De Boer H.A. Overmars H.R. Pomp E.L. Davis J.F. Zilverentant A. Goverse G. Smant J.P.W.G. Stokkermans R.S. Hussey F.J. Gommers J. Bakker A. Schots (1996) ArticleTitleProduction and characterization of monoclonal antibodies to antigens from second-stage juveniles of the potato cyst-nematode, Globodera rostochiensis Fundam. Appl. Nematol. 19 545–54

    Google Scholar 

  • D.I. De Pomerai (1996) ArticleTitleHeat-shock proteins as biomarkers of pollution Hum. Exp. Toxicol. 15 279–85 Occurrence Handle10.1177/096032719601500401 Occurrence Handle8845215 Occurrence Handle1:CAS:528:DyaK28XivFyrs7o%3D

    Article  PubMed  CAS  Google Scholar 

  • D. Drobne S.P. Hopkin (1995) ArticleTitleThe toxicity of zinc to terrestrial isopods in a “standard” laboratory test Ecotoxicol. Environ. Safety 31 1–6 Occurrence Handle7544260 Occurrence Handle1:CAS:528:DyaK2MXmtVKjurY%3D

    PubMed  CAS  Google Scholar 

  • D.Y. Dunlap F. Matsumura (1997) ArticleTitleDevelopment of broad spectrum antibodies to heat shock protein 70s as biomarkers for detection of multiple stress by pollutants and environmental factors Ecotoxicol. Environ. Safety 37 238–44 Occurrence Handle9378090 Occurrence Handle1:CAS:528:DyaK2sXmvVWmsb8%3D

    PubMed  CAS  Google Scholar 

  • H. Eckwert G. Alberti H.-R. Köhler (1997) ArticleTitleThe induction of stress proteins (hsp) in Oniscus asellus (Isopoda) as a molecular marker of multiple heavy metal exposure: I. Principles and toxicological assessment Ecotoxicology 6 249–62 Occurrence Handle1:CAS:528:DyaK2sXntVSru78%3D

    CAS  Google Scholar 

  • Eisenbeis, G. (1993). Zersetzung im Boden. In R. Ehrnsberger (ed.). Bodenmesofauna und Naturschutz Bedeutung und Auswirkungen von anthropogenen Maßnahmen. Inf. Natursch. Landschaftspfl. 6, 53–76.

  • R.J. Ellis S.M. van der Vies (1991) ArticleTitleMolecular chaperones Annu. Rev. Biochem. 60 321–47 Occurrence Handle1679318 Occurrence Handle1:CAS:528:DyaK3MXmtVWitbk%3D

    PubMed  CAS  Google Scholar 

  • P. Filzek D.J. Spurgeon G. Broll C. Svendsen P. Hankard J.E. Kammenga J.M. Weeks (2004) ArticleTitlePedological characterisation of sites along a transect from a primary cadmium/lead/zinc smelting works Ecotoxicology 13 725–737 Occurrence Handle15736845 Occurrence Handle1:CAS:528:DC%2BD2MXhslyrsrc%3D

    PubMed  CAS  Google Scholar 

  • M.-J. Gething J. Sambrook (1992) ArticleTitleProtein folding in the cell Nature 355 33–45 Occurrence Handle10.1038/355033a0 Occurrence Handle1:CAS:528:DyaK38XltlOqsg%3D%3D Occurrence Handle1731198

    Article  CAS  PubMed  Google Scholar 

  • Gräff, S. (1997). Ultrastrukturelle Plastizität und biochemische Biomarkerreaktionen sapro-/phytophager Bodeninvertebraten: Arbeiten zur Toxizität und Akkumulation umweltrelevanter Schadstoffe. Ph.D. thesis, University of Heidelberg, Heidelberg, F.R.G.

  • R.S. Gupta (1995) ArticleTitleEvolution of the chaperonin families (Hsp60, Hsp10 and Tcp-1) of proteins and the origin of eukaryotic cells Mol. Microbiol. 15 IssueID1 1–11 Occurrence Handle7752884 Occurrence Handle1:CAS:528:DyaK2MXjtVWlurY%3D

    PubMed  CAS  Google Scholar 

  • K. Guven J.A. Duce D.I. de Pomerai (1994) ArticleTitleEvaluation of a stress-inducible transgenic nematode strain for rapid aquatic toxicity testing Aquat. Toxicol. 29 119–37 Occurrence Handle1:CAS:528:DyaK2cXltVWgsb0%3D

    CAS  Google Scholar 

  • S.M. Hemmingsen C. Woolford S.M. van der Vies K. Tilly D.T. Dennis C.P. Georgopoulos R.W. Hendrix R.J. Ellis (1988) ArticleTitleHomologous plant and bacterial proteins chaperone oligomeric protein assembly Nature 333 330–4 Occurrence Handle2897629 Occurrence Handle1:CAS:528:DyaL1cXmt1Cqtbo%3D

    PubMed  CAS  Google Scholar 

  • L.E. Hightower (1993) ArticleTitleA brief perspective on the heat-shock response and stress proteins Marine Environ. Res. 35 79–83 Occurrence Handle1:CAS:528:DyaK3sXit1yhu7k%3D

    CAS  Google Scholar 

  • S.P. Hopkin (1989) Ecophysiology of Metals in Terrestrial Invertebrates Elsevier London, UK

    Google Scholar 

  • S.P. Hopkin (1990) ArticleTitleSpecies-specific differences in the net assimilation of zinc, cadmium, lead, copper and iron by the terrestrial isopods Oniscus asellus and Porcellio scaber J. Appl. Ecol. 27 460–74

    Google Scholar 

  • S.P. Hopkin C.A.C. Hames (1994) ArticleTitleZinc among a ‘cocktail’ of metal pollutants, is responsible for the absence of the terrestrial isopod Porcellio scaber from the vicinity of a primary smelting works Ecotoxicology 2 68–78

    Google Scholar 

  • J.E. Kammenga M.S.J. Arts W.J.M. Oude-Breuil (1998) ArticleTitleHSP60 as a potential biomarker of toxic stress in the nematode Plectus acuminatus Arch. Environ. Contam. Toxicol. 34 253–58 Occurrence Handle9504972 Occurrence Handle1:CAS:528:DyaK1cXhvFKmtrs%3D

    PubMed  CAS  Google Scholar 

  • J.E. Kammenga P.H.G. Van Koert J.A.G. Riksen G.W. Korthals J. Bakker (1996) ArticleTitleA toxicity test in artificial soil based on the life-history strategy of the nematode Plectus acuminatus Environ. Toxicol. Chem. 15 IssueID5 722–27 Occurrence Handle1:CAS:528:DyaK28XislCktL0%3D

    CAS  Google Scholar 

  • H.-R. Köhler H. Eckwert (1997) ArticleTitleThe induction of stress proteins (hsp) in Oniscus asellus (Isopoda) as a molecular marker of multiple heavy metal exposure. II: Joint toxicity and transfer to field situations Ecotoxicology 6 263–74

    Google Scholar 

  • H.-R. Köhler H. Eckwert R. Triebskorn G. Bengtsson (1999b) ArticleTitleInteraction between tolerance and 70 kDa stress protein (hsp70) induction in collembolan populations exposed to long-term metal pollution Appl. Soil Ecol. 11 43–52

    Google Scholar 

  • H.-R. Köhler C. Knödler M. Zanger (1999a) ArticleTitleDivergent kinetics of hsp70 induction in Oniscus asellus (Isopoda) in response to four environmentally relevant organic chemicals (B[a]P, PCB52, γ-HCH, PCP): Suitability and limits of a biomarker Arch. Environ. Contam. Toxicol. 36 179–85

    Google Scholar 

  • H.-R. Köhler R. Triebskorn W. Stöcker P.-M. Kloetzel G. Alberti (1992) ArticleTitleThe 70 kD heat shock protein (hsp70) in soil invertebrates: a possible tool for monitoring environmental toxicants Arch. Environ. Contam. Toxicol. 22 334–38 Occurrence Handle1616318

    PubMed  Google Scholar 

  • H.-R. Köhler M. Zanger H. Eckwert I. Einfeldt (2000) ArticleTitleSelection favours low hsp70 levels in chronically metal-stressed soil arthropods J. Evol. Biol. 13 569–82

    Google Scholar 

  • U.K. Laemmli (1970) ArticleTitleCleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 227 680–85 Occurrence Handle5432063 Occurrence Handle1:CAS:528:DC%2BD3MXlsFags7s%3D

    PubMed  CAS  Google Scholar 

  • S. Lindquist (1986) ArticleTitleThe heat-shock response Annu. Rev. Biochem. 55 1151–91 Occurrence Handle2427013 Occurrence Handle1:CAS:528:DyaL28XltV2lsrY%3D

    PubMed  CAS  Google Scholar 

  • S. Lindquist E.A. Craig (1988) ArticleTitleThe heat-shock proteins Annu. Rev. Genet. 22 631–77 Occurrence Handle2853609 Occurrence Handle1:CAS:528:DyaL1MXhtlSmtbg%3D

    PubMed  CAS  Google Scholar 

  • F. Mariño C. Winters A.J. Morgan (1999) ArticleTitleHeat shock protein (hsp60, hsp70, hsp90) expression in earthworms exposed to metal stressors in the field and laboratory Pedobiologia 43 615–24

    Google Scholar 

  • L. Nover (1991) The Heat Shock Response CRC Press Boca Raton 509

    Google Scholar 

  • D.A. Parsell S. Lindquist (1993) ArticleTitleThe function of heat-shock proteins in stress tolerance: Degradation and reactivation of damaged proteins Annu. Rev. Genet. 27 437–96 Occurrence Handle8122909 Occurrence Handle1:CAS:528:DyaK2cXhvVGnt7o%3D

    PubMed  CAS  Google Scholar 

  • L. Posthuma N.M. van Straalen (1993) ArticleTitleHeavy metal adaptation in terrestrial invertebrates: a review of occurrence, genetics, physiology and ecological consequences Comp. Biochem. Physiol. 106C 11–38 Occurrence Handle1:CAS:528:DyaK3sXms1Chs78%3D

    CAS  Google Scholar 

  • E. Pyza P. Mak P. Kramarz R. Laskowski (1997) ArticleTitleHeat shock proteins (HSP70) as biomarkers in exotoxicological studies Ecotoxicol. Environ. Safety 38 244–51 Occurrence Handle9469876 Occurrence Handle1:CAS:528:DyaK1cXhtlWjsLw%3D

    PubMed  CAS  Google Scholar 

  • F. Ritossa (1962) ArticleTitleA new puffing pattern induced by temperature shock and DNP in Drosophila Experientia 18 571–573 Occurrence Handle1:CAS:528:DyaF3sXivVOgtw%3D%3D

    CAS  Google Scholar 

  • B.M. Sanders (1990) Stress proteins: potential as multitiered biomarkers J.F. McCarthy L.R. Shugart (Eds) Biomarkers of Environmental Contamination Lewis Publishers Chelsea, MI 165–91

    Google Scholar 

  • B.M. Sanders (1993) ArticleTitleStress proteins in aquatic organisms: an environmental perspective Crit. Rev. Toxicol. 23 IssueID1 49–75 Occurrence Handle8471160 Occurrence Handle1:CAS:528:DyaK3sXkt1Crs7Y%3D

    PubMed  CAS  Google Scholar 

  • R.O. Schill H.-R. Köhler (2004) ArticleTitleEnergy reserves and metal-storage granules in the hepatopancreas of Oniscus asellus and Porcellio scaber (Isopoda) from a metal gradient at Avonmouth, UK Ecotoxicology 13 787–796 Occurrence Handle15736849 Occurrence Handle1:CAS:528:DC%2BD2MXhslyrs70%3D

    PubMed  CAS  Google Scholar 

  • Schouten, A.J. and Van der Brugge, I.R. (1989). Acute toxiciteit van aluminium en H + -ionen concentratie voor bodemnematoden uit een zuur en kalkrijk dennenbos. 1) Ontwikkeling en toepassing van een toets in waterig medium. National Institute of Public Health and Environmental Protection, Bilthoven, The Netherlands, Report nr. 718603001.

  • D.R. Spitz G.C. Li (1990) ArticleTitleHeat-induced cytotoxicity in hydrogen peroxide-resistant Chinese hamster fibroblasts J. Cell. Physiol. 142 255–60 Occurrence Handle2303525 Occurrence Handle1:CAS:528:DyaK3cXhtlKls70%3D

    PubMed  CAS  Google Scholar 

  • H. Towbin S. Theophil J. Gordon (1979) ArticleTitleElectrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications Proc. Natl. Acad. Sci. USA 76 4350–54 Occurrence Handle388439 Occurrence Handle1:CAS:528:DyaE1MXmtVKltLw%3D

    PubMed  CAS  Google Scholar 

  • Van Bezooijen, J. (1997). Methoden en technieken voor nematologie, 95 pp. Landbouwuniversiteit Wageningen, Vakgroep Nematologie.

  • W.J. Welch (1993) ArticleTitleHow cells respond to stress Sci. Am. 1993 IssueID5 34–41

    Google Scholar 

  • C.E. Wheelock M.F. Wolfe H. Olsen R.S. Tjeerdema M.L. Sowby (1999) ArticleTitleHsp60-induced tolerance in the rotifer Brachionus plicatilis exposed to multiple environmental contaminants Arch. Environ. Contam. Toxicol. 36 281–87 Occurrence Handle10047595 Occurrence Handle1:CAS:528:DyaK1MXhs1OltrY%3D

    PubMed  CAS  Google Scholar 

  • S. Wickner J. Hoskins K. McKenny (1991) ArticleTitleFunction of DnaJ and DnaK as chaperones in origin-specific DNA binding by RepA Nature 350 165–67 Occurrence Handle10.1038/350165a0 Occurrence Handle1:CAS:528:DyaK3MXhvVSnu74%3D Occurrence Handle2005967

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Author notes

  1. Ralph O. Schill, Thomas Knigge & Heinz-R. KÖhler

    Present address: Animal Physiological Ecology, Zoological Institute, University of Tübingen, Konrad-Adenauer-Str. 20, D-72072, Tübingen, Germany

Authors and Affiliations

  1. Laboratory of Nematology, Wageningen University, Binnenhaven 5, NL-6709 PD, Wageningen, The Netherlands

    Marie-José S. J. Arts & Jan E. Kammenga

  2. Cell Biology, Zoological Institute, University of Tübingen, Auf der Morgenstelle 28, D-72076, Tübingen, Germany

    Ralph O. Schill, Thomas Knigge, Helga Eckwert & Heinz-R. KÖhler

Authors
  1. Marie-José S. J. Arts
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ralph O. Schill
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Thomas Knigge
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Helga Eckwert
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jan E. Kammenga
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Heinz-R. KÖhler
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Heinz-R. KÖhler.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Arts, MJ.S.J., Schill, R.O., Knigge, T. et al. Stress Proteins (hsp70, hsp60) Induced in Isopods and Nematodes by Field Exposure to Metals in a Gradient near Avonmouth, UK. Ecotoxicology 13, 739–755 (2004). https://doi.org/10.1007/s10646-003-4473-5

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-003-4473-5

Keywords

Search

Navigation