Skip to main content
SpringerLink
Log in

Could contaminant induced mutations lead to a genetic diversity overestimation?

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

Contaminant driven genetic erosion reported through the inspection of selectable traits can be underestimated using neutral markers. This divergence was previously reported in the aquatic system of an abandoned pyrite mine. The most sensitive genotypes of the microcrustacean cladoceran Daphnia longispina were found to be lacking in the impacted reservoir near the entrance of the metal rich acid mine drainage (AMD). Since that divergence could be, at least partially, accounted for by mutagenicity and genotoxicity of the AMD, the present study aimed at providing such a characterization. The Allium cepa chromosomal aberration assay, using root meristematic cells, was carried out, by exposing seeds to 100, 10, 1, and 0.1 % of the local AMD. Chromosomal aberrations, cell division phases and cell death were quantified after the AMD exposure and after 24 and 48 h recovery periods. The AMD revealed to be mutagenic and genotoxic, even after diluting it to 1 and 0.1 %. Dilutions within this range were previously found to be below the lethality threshold and to elicit sublethal effects on reproduction of locally collected D. longispina clonal lineages Significant mutagenic effects (micronuclei and chromosomal breaks) were also found at 0.1 % AMD, supporting that exposure may induce permanent genetic alterations. Recovery tests showed that AMD genotoxic effects persisted after the exposure.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Aaron CS, Yu RL, Bacon JA, Kirkland D, McEnaney S, Marshall R (1995) Comparative mutagenicity testing of ceftiofur sodium II. Cytogenitic damage induced in vitro by ceftiofur is reversible and is due to cell cycle delay. Mutat Res-Genet Toxicol Environ 345:37–47

    Article  CAS  Google Scholar 

  • Agra AR, Guilhermino L, Soares AM, Barata C (2010) Genetic costs of tolerance to metals in Daphnia longispina populations historically exposed to a copper mine drainage. Environ Toxicol Chem 29:939–946

    Article  CAS  Google Scholar 

  • Agra AR, Soares AMVM, Barata C (2011) Life-history consequences of adaptation to pollution. Daphnia longispina clones historically exposed to copper? Ecotoxicology 20:552–562

    Article  CAS  Google Scholar 

  • Au WW, Cantelli –Forti G, Hrelia P, Legator MS (1990) Cytogenetic assays in genotoxic studies: somatic cell effects of benzene and germinal cell effects of dibromochloropropane. Teratogen Carcin Mutagen 10:125–134

    Article  CAS  Google Scholar 

  • Aydinalp C, Marinova S (2009) The effects of heavy metals on seed germination and plant growth on alfalfa plant (Medicago sativa). Bulg J Agric Sci 15:347–350

    Google Scholar 

  • Baker AJM (1987) Metal tolerance. New Phytol 106:93–111

    Article  CAS  Google Scholar 

  • Bewley JD (1997) Seed germination and dormancy. Plant Cell 9:1055–1066

    Article  CAS  Google Scholar 

  • Caritá R, Marin-Morales MA (2008) Induction of chromosome aberrations in the Allium cepa test system caused by the exposure of seeds to industrial effluents contaminated with azo dyes. Chemosphere 72:722–725

    Article  Google Scholar 

  • Chauhan LKS, Saxena PN, Gupta SK (1999) Cytogenetic effects of cypermethrin and fenvalerate on the root meristem cells of Allium cepa. Environ Exp Bot 42:181–189

    Article  CAS  Google Scholar 

  • Cho M, Chardonnens AN, Dietz K-J (2003) Differential heavy metal tolerance of Arabidopsis halleri and Arabidopsis thaliana: a leaf slice test. New Phytol 158:287–293

    Article  CAS  Google Scholar 

  • De Bisthoven LJ, Gerhardt A, Soares AMVM (2004) Effects of acid mine drainage on larval Chironomus (Diptera, Chironomidae) measured with the multispecies freshwater Biomonitor®. Environ Toxicol Chem 23:1123–1128

    Article  Google Scholar 

  • Dearfield KL, Cimino MC, McCarroll NE, Mauer I, Valcovic LR (2002) Genotoxicity risk assessment: a proposed classification strategy. Mutat Res-Gen Toxicol Environ 521:121–135

    Article  CAS  Google Scholar 

  • Fernandes TCC, Mazzeo DEC, Marin-Morales MA (2007) Mechanism of micronuclei formation in polyploidizated cells of Allium cepa exposed to trifluralin herbicide. Pestic Biochem Physiol 88:252–259

    Article  CAS  Google Scholar 

  • Fernandes TCC, Mazzeo DEC, Marin-Morales MA (2009) Origin of nuclear and chromosomal alterations derived from the action of an aneugenic agent—Trifluralin herbicide. Ecotoxicol Environ Saf 72:1680–1686

    Article  CAS  Google Scholar 

  • Fiskesjö G (1985) The Allium test as a standard in environmental monitoring. Hereditas 102:99–112

    Article  Google Scholar 

  • Fiskesjö G (1993) The Allium test in wastewater monitoring. Environ Toxicol Water 8:291–298

    Article  Google Scholar 

  • Gerhardt A, Janssens de Bisthoven L, Soares AMVM (2005) Effects of acid mine drainage and acidity on the activity of Choroterpes picteti (Ephemeroptera: leptophlebiidae). Arch Environ Contam Toxicol 48:450–458

    Article  CAS  Google Scholar 

  • Grant WF (1994) The present status of higher plant bioassays for the detection of environmental mutagens. Mutat Res-Fund Mol Mech 310:175–185

    Article  CAS  Google Scholar 

  • Grant WF (1998) Higher plant assays for the detection of genotoxicity in air polluted environments. Ecosyst Health 4:210–229

    Article  Google Scholar 

  • Grant WF (1999) Higher plant assays for the detection of chromosomal aberrations and gene mutations: a brief historical background on their use for screening and monitoring environmental chemicals. Mutat Res-Fund Mol M 426:107–112

    Article  CAS  Google Scholar 

  • Gustavino B, Scornajenghi KA, Minissi S, Ciccotti E (2001) Micronuclei induced in erythrocytes of Cyprinus carpio (Teleostei, Pisces) by X-rays and colchicine. Mutat Res-Gen Tox Env 494:151–159

    Article  CAS  Google Scholar 

  • Heddle JA, Cimino MC, Hayashi M, Romagna F, Shelby MD, Tucker JD, Vanparys P, MacGregor JT (1991) Micronuclei as an index of cytogenetic damage: past, present, and future. Environ Mol Mutagen 18:277–291

    Article  CAS  Google Scholar 

  • HERAG (2007) Mutagenicity. Health Risk Assessment Guidance For Metals Fact Sheet 05

  • Houk VS (1992) The genotoxicity of industrial wastes and effluents: a review. Mutat Res-Rev Genet 277:91–138

    Article  CAS  Google Scholar 

  • Huang Y, Jiang L, Yi Q, Lv L, Wang Z, Zhao X, Zhong L, Jiang H, Rasool S, Hao Q, Guo Z, Cooke HJ, Fenech M, Shi Q (2012) Lagging chromosomes entrapped in micronuclei are not ‘lost’ by cells. Cell Res 22:932–935

    Article  CAS  Google Scholar 

  • John R, Ahmad P, Gadgil K, Sharma S (2009) Heavy metal toxicity: effect on plant growth, biochemical parameters and metal accumulation by Brassica juncea L. Int J Plant Prod 3:65–76

    CAS  Google Scholar 

  • Kirkland D (1998) Chromosome aberration testing in genetic toxicology: past, present and future. Mutat Res-Fund Mol Mech 404:173–185

    Article  CAS  Google Scholar 

  • Komissarova EV, Saha SK, Rossman TG (2005) Dead or dying: the importance of time in cytotoxicity assays using arsenite as an example. Toxicol Appl Pharm 202:99–107

    Article  CAS  Google Scholar 

  • Kroemer G, Galluzzi L, Vandenabeele P, Abrams J, Alnemri E, Baehrecke E, Blagosklonny M, El-Deiry W, Golstein P, Green D, Hengartner M, Knight R, Kumar S, Lipton S, Malorni W, Nuñez G, Peter M, Tschopp J, Yuan J, Piacentini M, Zhivotovsky B, Melino G (2009) Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ 16:3–11

    Article  CAS  Google Scholar 

  • Leme DM, Marin-Morales MA (2009) Allium cepa test in environmental monitoring: a review on its application. Mutat Res-Rev Mutat 682:71–81

    Article  CAS  Google Scholar 

  • Leme DM, Angelis DdFd, Marin-Morales MA (2008) Action mechanisms of petroleum hydrocarbons present in waters impacted by an oil spill on the genetic material of Allium cepa root cells. Aquat Toxicol 88:214–219

    Article  CAS  Google Scholar 

  • Lerda D (1992) The effect of lead on Allium cepa L. Mutat Res Lett 281:89–92

    Article  CAS  Google Scholar 

  • Lin J, Jiang W, Liu D (2003) Accumulation of copper by roots, hypocotyls, cotyledons and leaves of sunflower (Helianthus annuus L.). Bioresource Technol 86:151–155

    Article  CAS  Google Scholar 

  • Liu C, Shen Z, Li X (2007) Accumulation and detoxification of cadmium in Brassica pekinensis and B. chinensis. Biol Plantarum 51:116–120

    Article  CAS  Google Scholar 

  • Lopes I, Gonçalves F, Soares AMVM, Ribeiro R (1999) Discriminating the ecotoxicity due to metals and to low pH in acid mine drainage. Ecotoxicol Environ Saf 44:207–214

    Article  CAS  Google Scholar 

  • Lopes I, Baird DJ, Ribeiro R (2005) Resistance to metal contamination by historically-stressed populations of Ceriodaphnia pulchella: environmental influence versus genetic determination. Chemosphere 61:1189–1197

    Article  CAS  Google Scholar 

  • Ma T-H, Cabrera Guillermo L, Owens E (2005) Genotoxic agents detected by plant bioassays. Rev Environ Health 20:1–13

    Article  CAS  Google Scholar 

  • Majno G, Joris I (1995) Apoptosis, oncosis, and necrosis. An overview of cell death. Am J Pathol 146:3–15

    CAS  Google Scholar 

  • Martins N, Lopes I, Guilhermino L, Bebianno MJ, Ribeiro R (2005) Lack of evidence for metallothionein role in tolerance to copper by natural populations of Daphnia longispina. Bull Environ Contam Toxicol 74:761–768

    Article  CAS  Google Scholar 

  • Martins N, Lopes I, Harper RM, Ross P, Ribeiro R (2007) Differential resistance to copper and mine drainage in Daphnia longispina: relationship with allozyme genotypes. Environ Toxicol Chem 26:1904–1909

    Article  CAS  Google Scholar 

  • Martins N, Bollinger C, Harper RM, Ribeiro R (2009) Effects of acid mine drainage on the genetic diversity and structure of a natural population of Daphnia longispina. Aquat Toxicol 92:104–112

    Article  CAS  Google Scholar 

  • Mazzeo DEC, Fernandes TCC, Marin-Morales MA (2011) Cellular damages in the Allium cepa test system, caused by BTEX mixture prior and after biodegradation process. Chemosphere 85:13–18

    Article  CAS  Google Scholar 

  • Moreira-Santos M, Soares AMVM, Ribeiro R (2004) An in situ bioassay for freshwater environments with the microalga Pseudokirchneriella subcapitata. Ecotoxicol Environ Saf 59:164–173

    Article  CAS  Google Scholar 

  • Moreira-Santos M, Donato C, Lopes I, Ribeiro R (2008) Avoidance tests with small fish: determination of the median avoidance concentration and of the lowest-observed-effect gradient. Environ Toxicol Chem 27:1576–1582

    Article  CAS  Google Scholar 

  • Patra M, Sharma A (2002) Relative efficacy of Allium cepa and Allium sativum in anaphase–telophase test screening metal genotoxicity. Biologia 57:409–414

    CAS  Google Scholar 

  • Patra M, Bhowmik N, Bandopadhyay B, Sharma A (2004) Comparison of mercury, lead and arsenic with respect to genotoxic effects on plant systems and the development of genetic tolerance. Environ Exp Bot 52:199–223

    Article  CAS  Google Scholar 

  • Pereira EG, Moura I, Costa JR, Mahony JD, Thomann RV (1995) The S. Domingos Mine: a study of heavy metal contamination in the water column and sediments of the Chança River Basin by discharge from an ancient cupriferous pyrite mine (Portugal). Mar Freshwater Res 46:145–151

    CAS  Google Scholar 

  • Pereira AMM, Soares AMVM, Gonçalves F, Ribeiro R (2000) Water-column, sediment, and in situ chronic bioassays with cladocerans. Ecotoxicol Environ Saf 47:27–38

    Article  CAS  Google Scholar 

  • Pérez-Cadahía B, Laffon B, Porta M, Lafuente A, Cabaleiro T, López T, Caride A, Pumarega J, Romero A, Pásaro E, Méndez J (2008) Relationship between blood concentrations of heavy metals and cytogenetic and endocrine parameters among subjects involved in cleaning coastal areas affected by the ‘Prestige’ tanker oil spill. Chemosphere 71:447–455

    Article  Google Scholar 

  • Pfrender ME, Spitze K, Hicks J, Morgan K, Latta L, Lynch M (2000) Lack of concordance between genetic diversity estimates at the molecular and quantitative-trait levels. Conserv Genet 1:263–269

    Article  CAS  Google Scholar 

  • Rank J, Nielsen MH (1993) A modified Allium test as a tool in the screening of the genotoxicity of complex mixtures. Hereditas 118:49–53

    Article  CAS  Google Scholar 

  • Redmann RE, Abouguendia ZM (1979) Germination and seedling growth on substrates with extreme pH—Laboratory evaluation of buffers. J Appl Ecol 16:901–907

    Article  CAS  Google Scholar 

  • Ribeiro R, Lopes I (2013) Contaminant driven genetic erosion and associated hypotheses on alleles loss, reduced population growth rate and increased susceptibility to future stressors: an essay. Ecotoxicology 22 (in press). doi: 10.1007/s10646-013-1070-0

  • Ribeiro R, Baird DJ, Soares AMVM, Lopes I (2012) Contaminant driven genetic erosion: a case study with Daphnia longispina. Environ Toxicol Chem 31:977–982

    Article  CAS  Google Scholar 

  • Salter RM, McIlvaine TC (1920) Effect of reaction of solution on germination of seeds and on growth of seedlings. J Agr Res 19:73–95

    CAS  Google Scholar 

  • Saro L, Lopes I, Martins N, Ribeiro R (2012) Testing hypotheses on the resistance to metals by Daphnia longispina: differential acclimation, endpoints association, and fitness costs. Environ Toxicol Chem 31:909–915

    Article  CAS  Google Scholar 

  • Shoemaker CA, Carlson WH (1990) pH affects seed germination of eight bedding plant species. HortScience 25:762–764

    Google Scholar 

  • Silva RM, Pereira F, Carneiro J, Sobral O, Ribeiro R, Amorim A, Soares AMVM, Lopes I (2010) Microevolution in a natural population of Daphnia longispina exposed to acid mine drainage. In: N. Hamamura SS, S. Mendo, C. M. Barroso, H. Iwata and S. Tanabe (ed) Interdisciplinary studies on environmental chemistry—biological responses to contaminants, Terrapub, Tokyo, p 213–218

  • Smaka-Kincl V, Stegnar P, Lovka M, Toman MJ (1996) The evaluation of waste, surface and ground water quality using the Allium test procedure. Mutat Res-Genet Toxicol 368:171–179

    Article  CAS  Google Scholar 

  • Soudek P, Petrová Š, Vaněk T (2011) Heavy metal uptake and stress responses of hydroponically cultivated garlic (Allium sativum L.). Environ Exp Bot 74:289–295

    Article  CAS  Google Scholar 

  • Symeonidis L, Karataglis S (1992) Interactive effects of cadmium, lead and zinc on root growth of two metal tolerant genotypes Holcus lanatus L. Biometals 5:173–178

    Article  CAS  Google Scholar 

  • Turner GD, Lau RR, Young DR (1988) Effect of acidity on germination and seedling growth of Paulownia tomentosa. J Appl Ecol 25:561–567

    Article  Google Scholar 

  • Ulsh BA, Miller SM, Mallory FF, Mitchel REJ, Morrison DP, Boreham DR (2004) Cytogenetic dose–response and adaptive response in cells of ungulate species exposed to ionizing radiation. J Environ Radioactiv 74:73–81

    Article  CAS  Google Scholar 

  • Wagner A Jr, Santos CEM, Costa e Silva JO, Sobreira AR, Negreiros JRS (2006) Influence of soaking water pH and substrates in the seeds germination and initial development of the sweet passion fruit. R Bras Agrociência, Pelotas 12:231–235

    Google Scholar 

  • Whysner J, Vijayaraj Reddy M, Ross PM, Mohan M, Lax EA (2004) Genotoxicity of benzene and its metabolites. Mutat Res-Rev Mutat 566:99–130

    Article  CAS  Google Scholar 

  • Wong MH, Bradshaw AD (1982) A comparison of the toxicity of heavy metals, using root elongation of rye grass, Lolium perenne. New Phytol 91:255–261

    Article  CAS  Google Scholar 

  • Zar JH (2010) Biostatistical analysis. Pearson Prentice-Hall, Upper Saddle River, NJ

    Google Scholar 

Download references

Acknowledgments

This study was partially was funded by FSE and POPH by national funds through Fundação para a Ciência e a Tecnologia and Ministério da Ciência, Tecnologia e Ensino Superior (Ph.D. Grant SFRH/BD/28526/2006 to Olímpia Sobral).

Author information

Authors and Affiliations

  1. Department of Life Sciences, IMAR—Instituto do Mar, University of Coimbra, Apartado, 3046, 3001-401, Coimbra, Portugal

    Olímpia Sobral & Rui Ribeiro

  2. Departamento de Biologia, Instituto de Biociências de Rio Claro, Universidade Estadual Paulista Júlio de Mesquita Filho, SP, Brazil

    Maria Aparecida Marin-Morales

Authors
  1. Olímpia Sobral
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Maria Aparecida Marin-Morales
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rui Ribeiro
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rui Ribeiro.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sobral, O., Marin-Morales, M.A. & Ribeiro, R. Could contaminant induced mutations lead to a genetic diversity overestimation?. Ecotoxicology 22, 838–846 (2013). https://doi.org/10.1007/s10646-013-1079-4

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-013-1079-4

Keywords

Search

Navigation