Abstract
This study reveals out detoxifying and antioxidant enzyme response of Gammarus pulex exposed/polluted to chlorpyrifos-ethyl insecticide before and after biodegradation/bioremediation by Methylobacterium radiotolerans and Microbacterium arthrosphaerae. Cytochrome P450 1A1, glutathione S-transferase, catalase, and superoxide dismutase activities in G. pulex exposed to chlorpyrifos-ethyl before and after bioremediation/biodegradation by these two bacteria during 24 and 96 h tested by using commercial ELISA kits. The activity of catalase enzyme was decreased depending on chlorpyrifos-ethyl before and after bioremediation/biodegradation the enzyme activity was increased repeatedly. Superoxide dismutase activity level increased after chlorpyrifos-ethyl exposure in 96 h (p > 0.05). Following bioremediation, superoxide dismutase enzyme activity decreased again during 24 h (p > 0.05) and increased during 96 h (p < 0.05). Statistical differences were not found in cytochrome P450 1A1 enzyme activity before and after the process (p > 0.05). No significant differences were determined during the activity of glutathione S-transferase in 24 h (p > 0.05). The activities of glutathione S-transferase were increased after exposure of chlorpyrifos-ethyl during 96 h. After bioremediation; the activity of glutathione S-transferase increased even more (p < 0.05). The results determined that activities of G. pulex at superoxide dismutase, catalase, and glutathione S-transferase are common biomarkers for revealing out the efficiency of bioremediation of chlorpyrifos-ethyl with these two types of soil bacteria.
Similar content being viewed by others
Availability of data and materials
Not applicable.
References
Agrawa A, Sharma B (2010) Pesticide induced oxidative stress in mammalian systems. Int J Biol Med Res 1(3):90–104
Aksu O, Yildirim NC, Yildirim N, Danabas D, Danabas S (2015) Biochemical response of crayfish Astacus leptodactylus exposed to textile wastewater treated by indigenous white rot fungus Coriolus versicolor. Environ Sci Pollut Res 22:2987–2993
Altuntas I, Delibas N, Doguc DK, Ozmen S, Gultekin F (2003) Role of reactive oxygen species in organophosphate insecticide phosalone toxicity in erythrocytes in vitro. Toxicol in Vitro 17(2):153–157
Anwar WA (1997) Biomarker and human exposure to pesticides. Environ Health Perspect 105:801–806
APHA (1998) Standard methods for the examination of water and wastewater, 20th edn. American Public Health Association, Washington DC
Arias-Estevez M, Lopez-Periago E, Martinez-Carballo E, Simal-Gandara J, Mejuto JC, Garcia-Rio L (2008) The mobility and degradation of pesticides in soils and the pollution of groundwater resources. Agric Ecosyst Environ 123:247–260
Bacchetta C, Rossi AS, Ale A, Campana M, Parma J, Cazenave J (2014) Combined toxicological effects of pesticides: a fish multibiomarker approach. Ecol Indic 6:532–538
Barrett M (2000) The role of cytochrome P450 enzymes in herbicide metabolism. In: Cobbs AH, Kirkwood RC (eds) Herbicides and Their Mechanisms of Action. Sheffield Academic, Sheffield, pp 25–37
Birkhoj M, Nellemann C, Jarfelt K, Jacobsen H, Andersen HR, Dalggard M, Vinggaard AM (2004) The combined antiandrogenic effects of five commonly used pesticides. Toxicol Appl Pharmacol 15(201):10–20
Boryslawskyj M, Garrood AC, Pearson JT (1988) Elevation of GST as a stress response to organochlorine compounds in Sphaerium corneum. Mar Environ Res 24:101–104
Boschin GD, Agostina A, Arnoldi A, Marotta E, Zanardini E, Negri M, Valle A, Sorlini C (2003) Biodegradation of chlorsulfuron and metsulfuron- methyl by aspergillus niger in laboratory conditions. J Environ Sci Health B 38(6):737–746
Cemeli E, Baumgartner A, Anderson D (2009) Antioxidants and the Comet assay. Mutat Res Rev Mutat Res 681(1):51–67
Cremlyn R (1991) Agrochemicals: preparation and mode of action. Wiley, Chichester
De Lange HJ, Noordoven W, Murk AJ, Lürling MFLLW, Peeters ETHM (2006) Behavioural responses of Gammarus pulex (Crustacea, Amphipoda) to low concentrations of pharmaceuticals. Aquat Toxicol 78:209–216
Demirci O, Güven K, Asma D, Öğüt S, Uğurlu P (2018) Effects of endosulfan, thiamethoxam, and indoxacarb in combination with atrazine on multi-biomarkers in Gammarus kischineffensis. Ecotoxicol Environ Saf 147(218):749–758
Desaint S, Hartmann A, Parekh NR, Fournıer JC (2000) Genetic diversity of carbofuran-degrading soil bacteria. FEMS Microbiol Ecol 34(2):173–180
Dua M, Sıngh A, Sethunathan N, Johrı AK (2002) Biotechnology and bioremediation: successes and limitations. Appl Microbiol Biotechnol 59(2-3):143–152
Eaton DL, Daroff RB, Autrup H, Bridges J, Buffler P, Costa LG, Coyle J, McKhann G, Mobley WC, Nadel L, Neubert D, Schulte-Hermann R, Spencer PS (2008) Review of the toxicology of chlorpyrifos with an emphasis on human exposure and neurodevelopment. Crit Rev Toxicol 38:1–125
Erguven GO (2018) Comparison of some soil fungi in bioremediation of herbicide acetochlor under agitated culture media. Bull Environ Contam Toxicol 100:570–575
Erguven GO, Demir G (2019) Evaluation of the detoxification potential of Micrococcus strains and plants for bioremediate organochlorine herbicides. Int J Innov Approaches Agric Res 3(3):353–364
Erguven GO, Yildirim N (2016) Efficiency of some soil bacteria for chemical oxygen demand reduction of synthetic chlorsulfuron solutions under agitated culture conditions. Cell Mol Biol 62(6):92–96
Erguven GO, Yildirim N (2019) The evaluation of imidacloprid remediation in soil media by two bacterial strains. Curr Microbiol 76(12):1461–1466
Fang H, Wang Y, Gao C, Yan H, Dong B, Yu Y (2010) Isolation and characterization of Pseudomonas sp. CBW capable of degrading carbendazim. Biodegradation 21:939–946
Field J, Stams AM, Kato M, Schraa G (1995) Enhanced biodegradation of aromatic pollutants in cocultures of anaerobic and aerobic bacterial consortia. Anton Leeuw 67(1):47–77
Furukawa K (2003) Super bugs for bioremediation. Trends Biotechnol 21(5):187–190
Gerhardt A, Kienle C, Allan IJ, Greenwood R, Guigues N, Fouillac AM, Mills GA, Gonzalez C (2007) Biomonitoring with Gammarus pulex at the Meuse (NL), Aller (GER) and Rhine (F) rivers with the online Multispecies Freshwater Biomonitor®. J Environ Monit 9:979–985
Gui-Shan Z, Xiao-Ming J, Tian-Fan C, Xiao-Hang M, Yu-Hua Z (2005) Isolation and characterization of a new carbendazim-degrading Ralstonia sp. World J Microbiol Biotechnol 21:265–269
Gultekin F, Delibas N, Yasar S, Kilinc I (2001) In vivo changes in antioxidant systems and protective role of melatonin and a combination of vitamin C and Vitamin E on oxidative damage in erythrocytes induced by chlorpyrifos-ethyl in rats. Arch Toxicol 75:88–96
Hai DQ, Varga SI, Matkovics B (1997) Organophosphate effects of antioxidant system of carp (Cyprinus carpio) and catfish (Ictalurus nebulosus). Comp Biochem Physiol 117:83–88
Hemingway J (2000) The molecular basis of two contrasting metabolic mechanisms of insecticide resistance. Insect Biochem Mol Biol 30:1009–1015
James MO (1989) Biotransformation and disposition of PAH in aquatic invertebrates. In: Varanasi V (ed) Metabolism of polycyclic aromatic hydrocarbons in the aquatic environment. CRC Press, Boca Raton
Kono Y, Fridovich I (1982) Superoxide radicals inhibit catalase. J Biol Chem 257:5751–5754
Laemmli CM, Leveau JHJ, Zehnder AJB, Van der Meer JR (2000) Characterization of a second tfd gene cluster for chlorophenol and chlorocatechol metabolism on plasmid pJP4 in Ralstonia eutropha JMP134 (pJP4). J Bacteriol 182(15):4165–4172
Li X, Schuler MA, Berenbaum MR (2007) Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annu Rev Entomol 52:231–253
Lima PL, Benassi JC, Pedrosa RC, Dal Magro J, Oliveira TB, Wilhelm FD (2006) Time course variations of DNA damage and biomarkers of oxidative stress in Tilapia (Oreochromis niloticus) exposed to effluents from a swine industry. Arch Environ Contam Toxicol 50:23–30
Lu Z, Min H, Xia Y (2004) The response of Escherichia coli, Bacillus subtilis, and Burkholderia cepacia WZ1 to oxidative stress of exposure to quinclorac. J Environ Sci Health B 39:431–441
Maltby L, Crane M (1994) Responses of Gammarus pulex (Amphipoda, Crustacea) to metalliferous effluents: identification of toxic components and the importance of interpopulation variation. Environ Pollut 84:45–52
Mohamed MS (2009) Degradation of methomyl by the novel bacterial strain Stenotrophomonas maltophilia M1. EJB 12(4):1–6
Monteiro DA, de Almeida JA, Rantin FT, Kalinin AL (2006) Oxidative stress biomarkers in the freshwater characid fish, Brycon cephalus, exposed to organophosphorus insecticide Folisuper 600 (methyl parathion). Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 143(2):141–149
Motoyama N, Dauterman WC (1980) Glutathione S-transferases: their role in the metabolism of insecticides. Rev Biochem Toxicol 2:49–70
Mutch E, Daly AK, Williams FM (2007) The relationship between PON1 phenotype and PON1–192 genotype in detoxification of three oxons by human liver. Drug Metab Dispos 35:315–320
Oncu M, Gultekin F, Karaoz E, Altuntas I, Deliba N (2002) Nephrotoxicity in rats induced by chlorpyrifos-ethyl and ameliorating effects of antioxidants. Hum Exp Toxicol 21:223–230
Panda J, Kanjilal T, Das S (2018) Optimized biodegradation of carcinogenic fungicide carbendazim by Bacillus licheniformis JTC-3 from agro-effluent. Biotechnol Res Innov 2:45–57
Peixoto F, Alves-Fernandes D, Santos D, Fontainhas Fernandes A (2006) Toxicological effects of oxyfluorfen on oxidative stress enzymes in tilapia Oreochromis niloticus. Pestic Biochem Physiol 85:91–96
Prasad KVSK, Saradhi P, Sharmila P (1999) Concerted action of antioxidant enzymes and curtailed growth under zinc toxicity in Brassica juncea. Environ Exp Bot 42:1–10
Rewitz KF, Styrishave B, Løbner-Olsen A, Andersen O (2006) Marine invertebrate cytochrome P450: emerging insights from vertebrate and insects analogies. Comp Biochem Physiol C Toxicol Pharmacol 143:363–381
Sahinoz E, Aral F, Dogu Z, Koyuncu İ, Yuksekdag O (2019) The protective effects of curcumin on organophosphate insecticide chlorpyrifos-induced oxidative stress and DNA damage in Oncorhynchus mykiss. Turk J Fish Aquat Sci 20(3):185–195
Santos TG, Martinez CB (2012) Atrazine promotes biochemical changes and DNA damage in a Neotropical fish species. Chemosphere 89(9):1118–1125
Sayler GS, Hooper SW, Layton AC, King JMH (1990) Catabolic plasmids of environmental and ecological significance. Microb Ecol 19(1):1–20
Serdar O (2019) The effect of dimethoate pesticide on some biochemical biomarkers in pulex. Environ Sci Pol 26(21):21905–21914
Shi F, Jia X, Zhao C, Chen Y (2010) Antioxidant activities of various extracts from Artemisia selengensis Turcz (LuHao). Molecules 15:4934–4946
Song Y, Chen M, Zhou J (2017) Effects of three pesticides on superoxide dismutase and glutathione-S-transferase activities and reproduction of Daphnia magna. Arch Environ Prot 43(1):80–86
Tatar S, Yildirim NC, Serdar O, Erguven GO (2020) Can toxicities induced by insecticide methomyl be remediated via soil bacteria Ochrobactrum thiophenivorans and Sphingomonas melonis? Curr Microbiol 77:1301–1307
Timbrell JA, Draper R, Waterfield CJ (1994) Biomarkers in toxicology: new use of some old molecules? Toxicol Ecotoxicol News 1:4–14
World Health Organization (1986) Organophosphorus insecticides: a general introduction. Environmental Health Criteria, vol 63. WHO, Geneva
Xing H, Wang X, Sun G, Gao X, Xua S, Wang X (2012) Effects of atrazine and chlorpyrifos on activity and transcription of glutathione S-transferase in common carp (Cyprinus carpio L.). Environ Toxicol Pharmacol 33:233–244
Xu YG, Zhang JL, Li XF, Liu L (2013) Study on chronic toxicity of difenoconazole to Daphnia magna and its effect on GST enzymatic activity. Hubei Agric Sci 52:79–83
Yang Y, Cheng JZ, Singhal SS, Saini M, Pandya U, Awasthi S, Awasthi YC (2001) Role of glutathione S-transferases in protection against lipid peroxidation: overexpression of hGSTA2-2 in K562 cells protects against hydrogen peroxide induced apoptosis and inhibits Jnk and caspase 3 activation. J Biol Chem 276:19220–19230
Yildirim NC, Tanyol M, Yildirim N, Serdar O, Tatar S (2018) Biochemical responses of Gammarus pulex to malachite green solutions decolorized by Coriolus versicolor as a biosorbent under batch adsorption conditions optimized with response surface methodology. Ecotoxicol Environ Saf 30(156):41–47
Yildirim NC, Tanyol M, Serdar O, Yildirim N (2019) Gammarus pulex as a model organism to assess the residual toxicity of slaughterhouse wastewater treated by electrocoagulation process. Bull Envıron Contam Toxicol 103:447–452
Zelles L, Adrian P, Bai QY, Stepper K, Adrian MV, Fischer K, Maier A, Ziegler A (1991) Microbial activity measured in soils stored under different temperature and humidity conditions. Soil Biol Biochem 23:955–962
Author information
Authors and Affiliations
Contributions
GOE, OS, and NCY conceived and designed the research; GOE and OS studied at the field. GOE performed bioremediation assays. GOE, ST, OS, and NCY carried out the field measurements with laboratory analysis; NCY and ST studied enzymes. All of the authors performed statistical data analysis; GOE, OS, and NCY performed writing, review, and editing; GOE and NCY supervised the research; and all authors provided major input on the manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare that they have no competing interests.
Ethical approval
All authors declare that there is no ethical violation in this manuscript. Also, this manuscript does not contain data belonging to others.
Consent to participate
All authors have confirmed that this has not been published elsewhere and is currently not considered to be published elsewhere.
Consent to publish
All authors agree that the article can be published in Environmental Science and Pollution Research.
Additional information
Responsible editor: Philippe Garrigues
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Onder Erguven, G., Tatar, Ş., Serdar, O. et al. Evaluation of the efficiency of chlorpyrifos-ethyl remediation by Methylobacterium radiotolerans and Microbacterium arthrosphaerae using response of some biochemical biomarkers. Environ Sci Pollut Res 28, 2871–2879 (2021). https://doi.org/10.1007/s11356-020-10672-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-020-10672-9