Open Access Open Access  Restricted Access Subscription Access

Cellular and Molecular Basis of Heavy Metal-Induced Stress in Ciliates


Affiliations
1 Ciliate Biology Laboratory, Acharya Narendra Dev College, University of Delhi, Kalkaji, New Delhi 110 019, India
2 Maitreyi College, University of Delhi, Bapudham Complex, Chanakyapuri, New Delhi 110 021, India
 

Globally, heavy metals are the major pollutants present in both terrestrial and aquatic ecosystems. Increase in their concentration due to various anthropogenic activities is a matter of concern. Higher concentration of these metals is known to be toxic due to their non-biodegradable nature. Eukaryotic microorganisms, ciliates can be used as cellular tools to assess and study the various mechanisms to overcome heavy metal toxicity. Here we discuss, at cellular level, the effect of heavy metal toxicity on growth rate, behavioural and morphological changes of ciliates. At the molecular level, changes in stress genes like hsp70, metallothionein and expression of various antioxidant enzymes (superoxide dismutase, glutathione peroxidase) adopted by ciliates have also been deliberated. It is also being argued that ciliates can be used as biosensor/cellular tools for detecting heavy metal pollution.

Keywords

Ciliates, Heat Shock Protein, Heavy Metal Stress, Metallothionein, Superoxide Dismutase.
User
Notifications
Font Size

  • Tchounwou, P. B., Yedjou, C. G., Patiolla, A. K. and Sutton, D. J., Heavy metals toxicity and the environment. In Molecular, Clinical and Environmental Toxicology (ed. Luch, A.), Experientia Supplementum, Springer, Basel, 2012, vol. 101, pp. 133–164.
  • Gutierrez, J. C., Amaro, F. and Martin-Gonzalez, A., Heavy metal whole-cell biosensors using eukaryotic microorganisms: an updated critical review. Front. Microbiol., 2015, 6, 1–8.
  • Kim, H. S., Kim, Y. J. and Seo, Y. R., An overview of carcinogenic heavy metal: molecular toxicity mechanism and prevention. J. Cancer Prev., 2015, 20, 232–240.
  • Martin-Gonzalez, A., Diaz, S., Borniquel, S., Gallego, A. and Gutierrez, J. C., Cytotoxicity and bioaccumulation of heavy metals by ciliated protozoa isolated from urban wastewater treatment plants. Res. Microbiol., 2006, 157, 108–118.
  • Pudpong, S. and Chantangsi, C., Effects of four heavy metals on cell morphology and survival rate of the ciliate Bresslauides sp. Trop. Nat. Hist., 2015, 15, 117–125.
  • Twagilimana, L., Bohatier, J., Groliere, C. A., Bonnemoy, F. and Sargos, D., A new low-cost microbiotest with the protozoan Spirostomum teres: culture conditions and assessment of sensitivity of the ciliate to 14 pure chemicals. Ecotoxicol. Environ. Saf., 1998, 41, 231–244.
  • Gutierrez, J. C., Martin-Gonzalez, A., Diaz, S. and Ortega, R., Ciliates as a potential source of cellular and molecular biomarkers/biosensors for heavy metal pollution. Eur. J. Protistol., 2003, 39, 461–467.
  • Gutierrez, J. C., Martin-Gonzalez, A., Diaz, S., Amaro, F., Ortega, R., Gallego, A. and de Lucas, M. P., Ciliates as cellular tools to study the eukaryotic cell: heavy metal interactions. In Heavy Metal Pollution (eds Brown, S. E. and Welton, W. C.), Nova Science Publishers, New York, 2008, pp. 1–44.
  • Sauvant, M. P., Pepsin, D. and Piccinni, E., Tetrahymena pyriformis: a tool for toxicological studies. Chemosphere, 1999, 38, 1631–1639.
  • Rico, D., Martín-González, A., Díaz, S., de Lucas, P. and Gutiérrez, J. C., Heavy metals generate reactive oxygen species in terrestrial and aquatic ciliated protozoa. Comp. Biochem. Physiol., 2009, 49, 90–96.
  • Kim, S. H., Jung, M. Y. and Lee, Y. M., Effect of heavy metals on the antioxidant enzymes in the marine ciliate Euplotes crassus. Toxicol. Environ. Health Sci., 2011, 3, 213–219.
  • Coppellotti, O., Sensitivity to copper in a ciliate as a possible component of biological monitoring in the Lagoon of Venice. Arch. Environ. Contam. Toxicol., 1998, 35, 417–425.
  • Abraham, J. S., Sripoorna, S., Choudhary, A., Toteja, R., Gupta, R., Makhija, S. and Warren, A., Assessment of heavy metal toxicity in four species of freshwater ciliates (Spirotrichea : Ciliophora) from Delhi, India. Curr. Sci., 2017, 113, 2141–2150.
  • Diaz, S., Martin-Gonzalez, A. and Gutierrez, J. C., Evaluation of heavy metal acute toxicity and bioaccumulation in soil ciliated protozoa. Environ. Int., 2006, 32, 711–717.
  • Wanick, R. C., Paiva, T. D. S., de Carvalho, C. N. and de Silva-Neto, I. D., Acute toxicity of cadmium to freshwater ciliate Paramecium bursaria. Biociências, 2008, 16, 104–109.
  • Rehman, A., Shakoori, F. R. and Shakoori, A. R., Heavy metal resistant freshwater ciliate, Euplotes mutabilis, isolated from industrial effluents has potential to decontaminate wastewater of toxic metals. Bioresour. Technol., 2008, 99, 3890–3895.
  • Benlaifa, M., Djebar, M. R., Berredjem, H., Benamara, M., Ouali, K. and Djebar, H., Stress induced by cadmium: its effects on growth respiratory metabolism, antioxidant enzymes and reactive oxygen species (ROS) of Paramecium sp. Int. J. Pharm. Sci. Rev. Res., 2016, 38, 276–281.
  • Nicolau, A., Mota, M. and Lima, N., Physiological responses of Tetrahymena pyriformis to copper, zinc, cycloheximide and Triton-X-100. FEMS Microbiol. Ecol., 1999, 30, 209–216.
  • Dias, N. and Lima, N., A comparative study using a fluorescence-based and a direct-count assay to determine cytotoxicity in Tetrahymena pyriformis. Res. Microbiol., 2002, 153, 313–322.
  • Madoni, P. and Romeo, M. G., Acute toxicity of heavy metals towards freshwater ciliated protists. Environ. Pollut., 2006, 141, 1–7.
  • Gallego, A., Martín-González, A., Ortega, R. and Gutiérrez, J. C., Flow cytometry assessment of cytotoxicity and reactive oxygen species generation by single and binary mixtures of cadmium, zinc and copper on populations of the ciliated protozoan Tetrahymena thermophila. Chemosphere, 2007, 68, 647–661.
  • Olabarrieta, I., L’Azou, B., Yuric, J., Cambar, J. and Cajaraville, M. P., In vitro effects of cadmium on two different animal cell models. Toxicol. in vitro, 2001, 15, 511–517.
  • Jerka-Dziadosz, M. and Frankel, J., The effects of lithium chloride on pattern formation in Tetraymena thermophila. Dev. Biol., 1995, 171, 497–506.
  • Makhija, S., Gupta, R. and Toteja, R., Lithium-induced developmental anomalies in the spirotrich ciliate Stylonychia lemnae (Ciliophora, Hypotrichida). Eur. J. Protistol., 2015, 51, 290–298.
  • Krawczynska, W., Pivovarora, N. N. and Sobota, A., Effects of cadmium on growth, ultrastructure and content of chemical elements in Tetrahymena pyriformis and Acanthamoeba castellanii. Acta Protozool., 1989, 28, 245–252.
  • Coppellotti, O., Effects of cadmium on Uronema marinum (Ciliophora, Scuticociliatida) from Antarctica. Acta Protozool., 1994, 33, 159–167.
  • Iftode, E., Currgy, J. J., Fleury, A. and Fryd-Versavel, G., Action of a heavy metal ion, Cd++, on 2 ciliates, Tetrahymena pyriformis and Euplotes vannus. Acta Protozool., 1985, 24, 273–279.
  • Makhija, S., Gupta, R., Toteja, R., Abraham, J. S. and Sripoorna, S., Cadmium induced ultrastructural changes in the ciliate, Stylonychia mytilus (Ciliophora, Hypotrichida). J. Cell Tissue Res., 2015, 15, 5151–5157.
  • Pinot, F., Kreps, S. E., Bachelet, M., Hainaut, P., Bakonyi, M. and Polla, B. S., Cadmium in the environment: sources, mechanisms of biotoxicity and biomarkers. Rev. Environ. Health, 2000, 15, 299–323.
  • Martin-Gonzalez, A., Borniquel, S., Diaz, S., Ortega, R. and Gutierrez, J. C., Ultrastructural alterations in ciliated protozoa under heavy metal exposure. Cell Biol. Int., 2005, 29, 119–126.
  • Lafontaine, D. L. and Tollervey, D., The function and synthesis of ribosomes. Nature Rev. Mol. Cell Biol., 2001, 2, 514–520.
  • Shcherbik, N. and Pestov, D. G., Ubiquitin and ubiquitin-like proteins in the nucleolus: multitasking tools for a ribosome factory. Genes Cancer, 2010, 1, 681–689.
  • Shang, F. and Taylor, A., Ubiquitin–proteasome pathway and cellular responses to oxidative stress. Free Radic. Biol. Med., 2011, 51, 5–16.
  • Latonen, L., Moore, H. M., Bai, B., Jäämaa, S. and Laiho, M., Proteasome inhibitors induce nucleolar aggregation of proteasome target proteins and polyadenylated RNA by altering ubiquitin availability. Oncogene, 2011, 30, 790–805.
  • Gomes, A., Fernandes, E. and Lima, J. L. F. C., Fluorescece probes used for detection of reactive oxygen species. J. Biochem. Biophys. Methods, 2005, 65, 45–80.
  • Toteja, R., Makhija, S., Sripoorna, S., Abraham, J. S. and Gupta, R., Influence of copper and cadmium toxicity on antioxidant enzyme activity in freshwater ciliates. Indian J. Exp. Biol., 2017, 55, 694–701.
  • Pulido, M. D. and Parrish, A. R., Metal-induced apoptosis: mechanisms. Mutat. Res., 2003, 533, 227–241.
  • Caverzan, A., Passaia, G., Rosa, S. B., Ribeiro, C. W., Lazzarotto, F. and Margis-Pinheiro, M., Plant responses to stresses: role of ascorbate peroxidase in the antioxidant protection. Genet. Mol. Biol., 2012, 35, 1011–1019.
  • Jimenez, A., Hernandez, J. A., Pastori, G., del Rio, L. A. and Sevilla, F., Role of the ascorbate–glutathione cycle of mitochondria and peroxisomes in the senescence of pea leaves. Plant Physiol., 1998, 118, 1327–1335.
  • Hu, P. and Tirelli, N., Scavenging ROS: superoxide dismutase/catalase mimetics by the use of an oxidation-sensitive nanocarrier/enzyme conjugate. Bioconjugate Chem., 2012, 23, 438–449.
  • De Gara, L., de Pinto, M. C., Moliterni, V. M. C. and D’Egidio, M. G., Redox regulation and storage processes during maturation in kernels of Titranium duram. J. Exp. Bot., 2003, 54, 249–258.
  • Sies, H., Glutathione and its role in cellular functions. Free Radic. Biol. Med., 1999, 27, 916–921.
  • Shakoori, F. R., Zafar, M. F., Fatehullah, A., Rehman, A. and Shakoori, A. R., Response of glutathione level in a protozoan ciliate, Stylonychia mytilus, to increasing uptake of and tolerance to nickel and zinc in the medium. Pak. J. Zool., 2011, 43, 569–574.
  • Zitka, O. et al., Redox status expressed as GSH:GSSG ratio as a marker for oxidative stress in paediatric tumour patients. Oncol. Lett., 2012, 4, 1247–1253.
  • Schutzendübel, A. and Polle, A., Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J. Exp. Bot., 2002, 53, 1351–1365.
  • Thirumoorthy, N., Sunder, A. S., Kumar, K. T. M., Kumar. M. S., Ganesh, G. N. K. and Chatterjee, M., A review of metallothionein isoforms and their role in pathophysiology. World J. Surg. Oncol., 2011, 9, 54–60.
  • Zahid, M. T., Shakoori, F. R., Zulifqar, S., Ahmed, I., Al-Ghanim, K., Mehboob, S. and Shakoori, A. R., Molecular characterization of a copper metallothionein gene from a ciliate Tetrahymena farahensis. J. Cell. Biochem., 2016, 117, 1843–1854.
  • Ruttkay-Nedecky, B. et al., The role of metallothionein in oxidative stress. Int. J. Mol. Sci., 2013, 14, 6044–6066.
  • Minoru, H. et al., Tissue dependent preventive effect of metallothionein against DNA damage in dyslipidemic mice under repeated stresses of fasting or restraint. Life Sci., 2009, 84, 569–575.
  • Gutierrez, J. C., Amaro, F., Diaz, S., de Francisco, P., Cubas, L. L. and Martin-Gonzalez, A., Ciliate metallothioneins: unique microbial eukaryotic heavy-metal-binder molecules. J. Biol. Inorg. Chem., 2011, 16, 1025–1034.
  • Santovito, G., Formigari, A., Boldrin, F. and Piccinni, E., Molecular and functional evolution of Tetrahymena metallothioneins: new insights into the gene family of Tetrahymena thermophila. Comp. Biochem. Physiol. Part C, 2007, 144, 391–397.
  • Boldrin, F., Santovito, G., Irato, P. and Piccinni, E., Metal interaction and regulation of Tetrahymena pigmentosa metallothionein genes. Protist, 2002, 153, 283–291.
  • Shuja, R. N. and Shakoori, A. R., Identification, cloning and sequencing of a novel stress inducible metallothionein gene from locally isolated Tetrahymena tropicalis lahorensis. Gene, 2007, 405, 19–26.
  • Amaro, F., de Lucas, P., Martin‐Gonzalez, A. and Gutierrez, J. C., Two new members of the Tetrahymena multi‐stress‐inducible metallothionein family: characterization and expression analysis of T. rostrata Cd/Cu metallothionein genes. Gene, 2008, 423, 85–91.
  • Shuja, R. N. and Shakoori, A. R., Identification and cloning of first cadmium metallothionein like gene from locally isolated ciliate, Paramecium sp. Mol. Biol. Rep., 2009, 36, 549–560.
  • Dar, S., Shuja, R. N. and Shakoori, A. R., A synthetic cadmium metallothionein gene (PMCd1syn) of Paramecium species: expression, purification and characteristics of metallothionein protein. Mol. Biol. Rep., 2013, 40, 983–997.
  • De Francisco, P., Melgar, L. M., Díaz, S., Martin-Gonzalez, A. and Gutierrez, J. C., The Tetrahymena metallothionein gene family: twenty-one new cDNAs, molecular characterization, phylogenetic study and comparative analysis of the gene expression under different abiotic stressors. BMC Genomics, 2016, 17, 346.
  • Dong, G., Chen, H., Qi, M., Dou, Y. and Wang, Q., Balance between metallothionein and metal response element binding transcription factor 1 is mediated by zinc ions (review). Mol. Med. Rep., 2015, 11, 1582–1586.
  • Palmiter, R. D., Regulation of metallothionein genes by heavy metals appears to be mediated by a zinc-sensitive inhibitor that interacts with a constitutively active transcription factor, MTF-1. Proc. Natl. Acad. Sci. USA, 1994, 91, 1219–1223.
  • Saydam, N., Adams, T. K., Steiner, F., Schaffner, W. and Freedman, J. H., Regulation of metallothionein transcription by the metal-responsive transcription factor MTF-1. J. Biol. Chem., 2002, 277, 20438–20445.
  • Dondero, F., Cavaletto, M., Ghezzi, A. R., La Terza, A., Banni, M. and Viarengo, A., Biochemical characterization and quantitative gene expression analysis of the multi-stress inducible metallothionein from Tetrahymena thermophila. Protist, 2004, 155, 157–168.
  • Amaro, F., Turkewitz, A. P., Martín-González, A. and Gutiérrez, J. C., Whole-cell biosensors for detection of heavy metal ions in environmental samples based on metallothionein promoters from Tetrahymena thermophila. Microb. Biotechnol., 2011, 4, 513–522.
  • Res, P. C. M., Thole, J. E. R. and De Vries, R. R. P., Heat shock proteins in immunopathology. Curr. Opin. Immunol., 1991, 3, 924–929.
  • Hall, A. E., Crop Responses to Environment. CRC Press, Boca Raton, Florida, USA, 2001.
  • Parsell, D. A. and Lindquist, S., The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annu. Rev. Genet., 1993, 27, 437–496.
  • Feder, M. E. and Hofmann, G. E., Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu. Rev. Physiol., 1999, 61, 243–282.
  • Jung, M. Y. and Lee, Y. M., Expression profiles of heat shock protein gene families in the monogonont rotifer Brachionus koreanus – exposed to copper and cadmium. Toxicol. Environ. Health Sci., 2012, 4, 235–242.
  • Sonoda, S., Ashfaq, M. and Tsumuki, H., A comparison of heat shock protein genes from cultured cells of the cabbage armyworm, Mamestra brassicae, in response to heavy metals. Arch. Insect. Biochem. Physiol., 2007, 65, 210–222.
  • Javid, B., MacAry, P. A. and Lehner, P. J., Structure and function: heat shock proteins and adaptive immunity. J. Immunol., 2007, 179, 2035–2040.
  • Barchetta, S., La Terza, A., Ballarini, P., Pucciarelli, S. and Miceli, C., Combination of two regulatory elements in the Tetrahymena thermophila HSP70-1 gene controls heat shock activation. Eukaryot. Cell, 2008, 7, 379–386.
  • Olsson, B., Protein expression in Baltic Sea blue mussels exposed to natural and anthropogenic stress. Doctoral thesis in marine ecotoxicology, Department of Systems Ecology, Stockholm University, Stockholm, Sweden, 2005.
  • Zhang, Y., Dorey, S., Swiderski, M. and Jones, J. D., Expression of RPS4 in tobacco induces an AvrRps4-independent HR that requires EDS1, SGT1 and HSP90. Plant J., 2004, 40, 213–224.
  • Anderson, R. C., Lindauer, K. R. and Prescott, D. M., A gene-sized DNA molecule encoding heat-shock protein 70 in Oxytricha nova. Gene, 1996, 168, 103–107.

Abstract Views: 403

PDF Views: 118




  • Cellular and Molecular Basis of Heavy Metal-Induced Stress in Ciliates

Abstract Views: 403  |  PDF Views: 118

Authors

Sripoorna Somasundaram
Ciliate Biology Laboratory, Acharya Narendra Dev College, University of Delhi, Kalkaji, New Delhi 110 019, India
Jeeva Susan Abraham
Ciliate Biology Laboratory, Acharya Narendra Dev College, University of Delhi, Kalkaji, New Delhi 110 019, India
Swati Maurya
Ciliate Biology Laboratory, Acharya Narendra Dev College, University of Delhi, Kalkaji, New Delhi 110 019, India
Seema Makhija
Ciliate Biology Laboratory, Acharya Narendra Dev College, University of Delhi, Kalkaji, New Delhi 110 019, India
Renu Gupta
Maitreyi College, University of Delhi, Bapudham Complex, Chanakyapuri, New Delhi 110 021, India
Ravi Toteja
Ciliate Biology Laboratory, Acharya Narendra Dev College, University of Delhi, Kalkaji, New Delhi 110 019, India

Abstract


Globally, heavy metals are the major pollutants present in both terrestrial and aquatic ecosystems. Increase in their concentration due to various anthropogenic activities is a matter of concern. Higher concentration of these metals is known to be toxic due to their non-biodegradable nature. Eukaryotic microorganisms, ciliates can be used as cellular tools to assess and study the various mechanisms to overcome heavy metal toxicity. Here we discuss, at cellular level, the effect of heavy metal toxicity on growth rate, behavioural and morphological changes of ciliates. At the molecular level, changes in stress genes like hsp70, metallothionein and expression of various antioxidant enzymes (superoxide dismutase, glutathione peroxidase) adopted by ciliates have also been deliberated. It is also being argued that ciliates can be used as biosensor/cellular tools for detecting heavy metal pollution.

Keywords


Ciliates, Heat Shock Protein, Heavy Metal Stress, Metallothionein, Superoxide Dismutase.

References





DOI: https://doi.org/10.18520/cs%2Fv114%2Fi09%2F1858-1865