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Evaluation of oxidative stress biomarkers in Aiolopus thalassinus (Orthoptera: Acrididae) collected from areas polluted by the fertilizer industry

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Abstract

The waste products of the fertilizer industry such as heavy metals, but especially phosphates and sulphates, are a serious problem that influences the structure and functioning of ecosystems. The levels of Cd, Pb, Zn, Cu, sulphates and phosphates were measured in soil samples from four sites: a control and sites that were 1, 3 and 6 km (sites A–C) away from the Abu-Zaabal Fertilizer Company. Oxidative stress markers (protein carbonyls, lipid peroxides), antioxidant enzymes (superoxide dismutase (SOD), catalase (CAT), polyphenoloxidase (PPO) and ascorbate peroxidase (APOX)) were evaluated in the tissues of Aiolopus thalassinus, collected from the corresponding sites. The highest concentrations of Cu and Zn were found in the soil from site A. The level of protein carbonyls in the brain, thoracic muscles and gut of the males and females from sites A, B and C were 11.82, 4.38, 5.97 (males) and 19.04, 16.65, 7.79 (females) times higher, respectively, compared to the individuals from the control site. Lipid peroxides levels in both sexes were significantly correlated with the distance from the source of the contamination. In the brain, thoracic muscles and gut of the males and females collected from site A, the level of lipid peroxides were 15.41, 23.49, 11.50 (males) and 25.36, 11.34, 15.37 (females) times higher compared to the values of the control animals. The activities of SOD, PPO, CAT and APOX were significantly affected by the environmental pollutants. The enzymatic and non-enzymatic oxidative markers in the Aiolopus thalassinus, a common insect species that inhabits various ecosystems, can also be used as a relevant biomarker of the pollution that is caused by the fertilizer industry.

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References

  • Aebi H (1984) Catalase in vitro. Method Enzymol 105:121–126

    Article  CAS  Google Scholar 

  • Ahmad S (1992) Biochemical defense of pro-oxidant plant allelochemicals by herbivorous insects. Biochem Syst Ecol 20:269–296

    Article  CAS  Google Scholar 

  • Ahmed AM (2012) Lipid peroxidation and oxidative protein products as biomarkers of oxidative stress in the autogenous mosquito, Aedes caspius, upon infection with the mosquitocidal bacterium, Bacillus thuringiensis kurstaki. Pak J Zool 44:525–536

    CAS  Google Scholar 

  • Alves PRL, Cardoso EJBN (2016) Overview of the standard methods for soil ecotoxicology testing. In: Larramendy M, & Soloneski S (eds) Invertebrates—experimental models in toxicity screening. InTech, Croatia, pp 35–56. doi: 10.5772/62228

    Google Scholar 

  • Amado LL, Robaldo RB, Geracitano L, Monserrat JM, Bianchini A (2006) Biomarkers of exposure and effect in the Brazilian flounder Paralichthys orbignyanus (Teleostei: Paralichthyidae) from the Patos Lagoon estuary (Southern Brazil). Mar Pollut Bull 52:207–213

    Article  CAS  Google Scholar 

  • Asada K (1984) Chloroplasts: formation of active oxygen and its scavenging. Method Enzymol 105:422–429

    Article  CAS  Google Scholar 

  • Augustyniak M, Babczyńska A, Augustyniak M (2009a) Does the grasshopper Chorthippus brunneus adapt to metal polluted habitats? A study of glutathione-dependent enzymes in grasshopper nymphs. Insect Sci 16:33–42

    Article  CAS  Google Scholar 

  • Augustyniak M, Babczyńska A, Kozłowski M, Sawczyn T, Augustyniak M (2008) Effects of zinc and female aging on nymphal life history in a grasshopper from polluted sites. J Insect Physiol 54:41–50

    Article  CAS  Google Scholar 

  • Augustyniak M, Babczyńska A, Migula P, Wilczek G, Łaszczyca P, Kafel A, Augustyniak M (2005) Joint effects of dimethoate and heavy metals on metabolic responses in a grasshopper (Chorthippus brunneus) from a heavy metals pollution gradient. Comp Biochem Physiol 141:412–419

    Google Scholar 

  • Augustyniak M, Tarnawska M, Babczyńska A, Augustyniak M (2009b) Hsp70 level in progeny of aging grasshoppers from variously polluted habitats and additionally exposed to zinc during diapause. J Insect Physiol 55:735–741

    Article  CAS  Google Scholar 

  • Birben E, Sahiner UM, Sackesen C, Erzurum S, Kalayci O (2012) Oxidative stress and antioxidant defense. World Allergy Organ J 5:9–19

    Article  CAS  Google Scholar 

  • Boon DY, Soltanpour PN (1991) Estimating total lead cadmium and zinc in contaminated soils from ammonium bicarbonate 3-Dtpa-extractable levels. Commun Soil Sci Plant Anal 22:369

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  Google Scholar 

  • Carey C, Bryant CJ (1995) Possible interrelations among environmental toxicants, amphibian development, and decline of amphibian populations. Environ Health Perspect 103:13–17

    Article  CAS  Google Scholar 

  • Dalle-Donne I, Rossi R, Giustarini D, Milzani A, Colombo R (2003) Protein carbonyl groups as biomarkers of oxidative stress. Clin Chim Acta 329:23–38

    Article  CAS  Google Scholar 

  • Donahue JL, Okpodu CM, Cramer CL, Grabau EA, Alscher RG (1997) Responses of antioxidants to paraquat in pea leaves (relationships to resistance). Plant Physiol 113:249–257

    Article  CAS  Google Scholar 

  • Dos Anjos NA, Schulze T, Brack W, Val AL, Schirmer K, Scholz S (2011) Identification and evaluation of cyp1a transcript expression in fish as molecular biomarker for petroleum contamination in tropical fresh water ecosystems. Aquat Toxicol 103:46–52

    Article  Google Scholar 

  • Drevnick PE,  Sandheinrich MB (2003) Effects of Dietary Methylmercury on Reproductive Endocrinology of Fathead Minnows. Environ Sci  Technol 37(19):4390–4396

  • Dutta P, Dey T, Manna P, Kalita J (2016) Antioxidant potential of Vespa affinis L., a traditional edible insect species of North East India. PLoS One 11(5):e0156107. doi:10.1371/journal.pone.0156107

    Article  Google Scholar 

  • Fang YZ, Yang S, Wu G (2002) Free radicals, antioxidants, and nutrition. Nutrition 18:872–879

    Article  CAS  Google Scholar 

  • Farahat AA, Al-Sayed AA, Mahfoud NA (2010) Compost and other organic and inorganic fertilizers in the scope of the root-knot nematode reproduction and control. Egypt J Agronematol 9:18–29

    Google Scholar 

  • Farombi EO, Adelowo OA, Ajimoko YR (2007) Biomarkers of oxidative stress and heavy metal levels as indicators of environmental pollution in African cat fish (Clarias gariepinus) from Nigeria Ogun River. Int J Environ Res Public Health 4:158–165

    Article  CAS  Google Scholar 

  • Farooqui T, Farooqui AA (2011) Oxidative stress in vertebrates and invertebrates: molecular aspects of cell signaling. Wiley, Hoboken, New Jersey

    Book  Google Scholar 

  • Felton GW, Summers CB (1995) Antioxidant systems in insects. Arch Insect Biochem Physiol 29:187–197

    Article  CAS  Google Scholar 

  • Gilbert DL (2000) Fifty years of radical ideas. Ann N Y Acad Sci 899:1–14

    Article  CAS  Google Scholar 

  • Gutteridge JMC (1995) Lipid peroxidation and antioxidants as biomarkers of tissue damage. Clin Chem 41:1819–1828

    CAS  Google Scholar 

  • Halliwell B, Gutteridge JM (1984) Oxygen toxicity, oxygen radicals, transition metals and disease. Biochem J 219(1):1–14

    Article  CAS  Google Scholar 

  • Halliwell B, Gutteridge JM (2015) Free radical in biology & medicine. Oxford University Press, New York

    Book  Google Scholar 

  • Halliwell B, Whiteman M (2004) Measuring reactive species and oxidative damage in vivo and in cell culture: how should you do it and what do the results mean? Br J Pharmacol 142:231–255

    Article  CAS  Google Scholar 

  • Hermes-Lima M (2004) Oxygen in biology and biochemistry: role of free radicals. In: Storey KB (ed) Functional metabolism: regulation and adaptation. Wiley-Liss, Inc., Hoboken, New Jersey, pp 319–966

    Google Scholar 

  • Hermes-Lima M, Willmore WG, Storey KB (1995) Quantification of lipid peroxidation in tissue extracts based on Fe (III) xylenol orange complex formation. Free Radic Biol Med 19:271–280

    Article  CAS  Google Scholar 

  • Ihechiluru NB, Henry AN, Taiwo IE (2015) Heavy metal bioaccumulation and oxidative stress in Austroaeschna inermis (Dragon fly) of the lagos urban ecosystem. J Environ Chem Ecotoxicol 7:11–19

    Article  CAS  Google Scholar 

  • Kaviraj A, Unlu E, Gupta A, El Nemr A (2014) Biomarkers of environmental pollutants. Bio Med Res Int doi:10.1155/2014/806598

  • Kelly FJ, Mudway IS (2003) Protein oxidation at the air–lung interface. Amino Acids 25:375–396

    Article  CAS  Google Scholar 

  • Korsloot A, van Gestel CAM, van Straalen NM (2004) The oxidative stress response system. In: Korsloot A, van Gestel CAM, & van Straalen NM (Eds) Environmental stress and cellular response in arthropods. CRC Press, Boca Raton, Florida, pp 59–76

    Google Scholar 

  • Krishnan N, Kodrík D (2006) Antioxidant enzymes in Spodoptera littoralis (Boisduval): are they enhanced to protect gut tissues during oxidative stress? J Insect Physiol 52:11–20

    Article  CAS  Google Scholar 

  • Kumar KB, Khan PA (1982) Peroxidase and polyphenol oxidase in excised ragi (Eleusine corocana cv PR 202) leaves during senescence. Int J Exp Biol 20:412–416

    CAS  Google Scholar 

  • Levine RL, Garland D, Oliver CN, Amici A, Climent I, Lenz AG, Stadtman ER (1990) Determination of carbonyl content in oxidatively modified proteins. Method Enzymol 186:464–478

    Article  CAS  Google Scholar 

  • Lijun L, Xuemei L, Yaping G, Enbo M (2005) Activity of the enzymes of the antioxidative system in cadmium-treated Oxya chinensis (Orthoptera Acridoidae). Environ Toxicol Pharmacol 20:412–416

    Article  Google Scholar 

  • Livingstone DR (2001) Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. Mar Pollut Bull 42:656–666

    Article  CAS  Google Scholar 

  • Lushchak VI (2007) Free radical oxidation of proteins and its relationship with functional state of organisms. Biochemistry (Moscow) 72:809–827

    Article  CAS  Google Scholar 

  • Lushchak VI (2011) Environmentally induced oxidative stress in aquatic animals. Aquat Toxicol 101:13–30

    Article  CAS  Google Scholar 

  • Migula P, Łaszczyca P, Augustyniak M, Wilczek G, Rozpędek K, Kafel A, Wołoszyn M (2004) Antioxidative defence enzymes in beetles from a metal pollution gradient. Biol Bratisl 59:645–654

    CAS  Google Scholar 

  • Misra HP, Fridovich I (1972) The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem 247:3170–3175

    CAS  Google Scholar 

  • Nath S, Roy B, Bose S, Podder R (2015) Impact of arsenic on the cholinesterase activity of grasshopper. Am-Eurasian J Toxicol Sci 7:173–176

    Google Scholar 

  • Okamoto T, Taguchi M, Osaki T, Fukumoto S, Fujita T (2014) Phosphate enhances reactive oxygen species production and suppresses osteoblastic differentiation. J Bone Miner Metab 32:393–399

    Article  CAS  Google Scholar 

  • Piano A, Valbonesi P, Fabbri E (2004) Expression of cytoprotective proteins, heat shock protein 70 and metallothioneins, in tissues of Ostrea edulis exposed to heat and heavy metals. Cell Stress Chaperones 9:134–142

    Article  CAS  Google Scholar 

  • Pogue AI, Jones BM, Bhattacharjee S, Percy ME, Zhao Y, Lukiw WJ (2012) Metal-Sulfate induced generation of ROS in human brain cells: detection using an isomeric mixture of 5- and 6-carboxy-2′,7′-dichlorofluorescein diacetate (carboxy-DCFDA) as a cell permeant tracer. Int J Mol Sci 13:9615–9626

    Article  CAS  Google Scholar 

  • Radojevic M, Bashkin VN (1999) Practical environmental analysis. Royal Society of Chemistry, Cambridge

    Google Scholar 

  • Ray S (2016) Levels of toxicity screening of environmental chemicals using aquatic invertebrates - a review. In: Larramendy M, & Soloneski S (eds) Invertebrates—experimental models in toxicity screening. InTech, Croatia, pp 1–11. doi: 10.5772/61746

    Google Scholar 

  • Schmidt GH, Ibrahim NM (1994) Heavy metal content (Hg2+, Cd2+, Pb2+) in various body parts: its impact on cholinesterase activity and binding glycoproteins in the grasshopper Aiolopus thalassinus adults. Ecotoxicol Environ 29:148–164

    Article  CAS  Google Scholar 

  • Schmidt GH, Ibrahim NM, Abdallah MD (1992) Long-term effects of heavy metals in food on developmental stages of Aiolopus thalassinus (Saltatoria: Acrididae). Arch Environ Contam Toxicol 23:375–382

    Article  CAS  Google Scholar 

  • Sena LA, Chandel NS (2012) Physiological roles of mitochondrial reactive oxygen species. Mol Cell 48:158–167

    Article  CAS  Google Scholar 

  • Shinkai Y, Li S, Kikuchi T, Kumagai Y (2015) Participation of metabolic activation of 2, 4, 6-trinitrotoluene to 4-hydroxylamino-2, 6-dinitrotoluene in hematotoxicity. J Toxicol Sci 40:597–604

    Article  CAS  Google Scholar 

  • Sofo A, Scopa A, Nuzzaci M, Vitti A (2015) Review. Ascorbate peroxidase and catalase activities and their genetic regulation in plants subjected to drought and salinity stresses. Int J Mol Sci 16:13561–13578. doi:10.3390/ijms160613561

    Article  CAS  Google Scholar 

  • Soundararajan M, Veeraiyan G, Samipillai SS (2009) Arsenic-induced oxidative stress in fresh water catfish Tilapia Mossambica. J Phytol 1:267–276

    Google Scholar 

  • Sureda A, Box A, Enseñat M, Alou E, Tauler P, Deudero S, Pons A (2006) Enzymatic antioxidant response of a labrid fish (Coris julis) liver to environmental caulerpenyne. Comp Biochem Physiol 144:191–196

    Google Scholar 

  • USEPA (2014) Cleaning up the Nations Hazards Wastes Sites. United States Environmental Protection Agency. https://www.epa.gov/superfund/cleanup-optimization-superfund-sites

  • Winston GW (1991) Oxidants and antioxidants in aquatic animals. Comp Biochem Physiol 100:173–176

    CAS  Google Scholar 

  • Wuana RA, Okieimen FE (2011) Heavy metals in contaminated soils: a review of sources, chemistry, risks and best available strategies for remediation. ISRN Ecol. doi:10.5402/2011/402647

  • Yousef HA, Afify A, Hasan HM, Meguid AA (2010) DNA damage in hemocytes of Schistocerca gregaria (Orthoptera: Acrididae) exposed to contaminated food with cadmium and lead. . Nat Sci 02:292–297. doi:10.4236/ns.2010.24037

    CAS  Google Scholar 

  • Zhu H, Zhang J, Kim MT, Boison A, Sedykh A, Moran K (2014) Big data in chemical toxicity research: the use of high-throughput screening assays to identify potential toxicants. Chem Res Toxicol 27:1643–1651

    Article  CAS  Google Scholar 

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Acknowledgments

This study was funded by Cairo University, Faculty of Science, Egypt.

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Correspondence to Hesham A. Yousef.

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Yousef, H.A., Abdelfattah, E.A. & Augustyniak, M. Evaluation of oxidative stress biomarkers in Aiolopus thalassinus (Orthoptera: Acrididae) collected from areas polluted by the fertilizer industry. Ecotoxicology 26, 340–350 (2017). https://doi.org/10.1007/s10646-017-1767-6

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