Mechanisms of oxidative response during biodegradation of malathion by S. oneidensis MR-1.
Biotransformation
Cellular characteristics
Malathion
Oxidative stress
Shewanella spp
Journal
Environmental science and pollution research international
ISSN: 1614-7499
Titre abrégé: Environ Sci Pollut Res Int
Pays: Germany
ID NLM: 9441769
Informations de publication
Date de publication:
07 Feb 2024
07 Feb 2024
Historique:
received:
10
10
2023
accepted:
27
01
2024
medline:
8
2
2024
pubmed:
8
2
2024
entrez:
7
2
2024
Statut:
aheadofprint
Résumé
Malathion, an extensively used organophosphorus pesticide, poses a high potential risk of toxicity to humans and the environment. Shewanella (S.) oneidensis MR-1 has been proposed as a strain with excellent bioremediation capabilities, capable of efficiently removing a wide range of hard-to-degrade pollutants. However, the physiological and biochemical response of S. oneidensis MR-1 to malathion is unknown. Therefore, this study aimed to examine how S. oneidensis MR-1 responds physiologically and biochemically to malathion while also investigating the biodegradation properties of the pesticide. The results showed that the 7-day degradation rates of S. oneidensis MR-1 were 84.1, 91.6, and 94.0% at malathion concentrations of 10, 20, and 30 mg/L, respectively. As the concentration of malathion increased, superoxide dismutase and catalase activities were inhibited, leading to a significant rise in malondialdehyde content. This outcome can be attributed to the excessive production of reactive oxygen species (ROS) triggered by malathion stress. In addition, ROS production stimulates the secretion of soluble polysaccharides, which alleviates oxidative stress caused by malathion. Malathion-induced oxidative damage further exacerbated the changes in the cellular properties of S. oneidensis MR-1. During the initial stages of degradation, the cell density and total intracellular protein increased significantly with increasing malathion exposure. This can be attributed to the remarkable resistance of S. oneidensis MR-1 to malathion. Based on scanning electron microscopy observations, continuous exposure to contaminants led to a reduction in biomass and protein content, resulting in reduced cell activity and ultimately leading to cell rupture. In addition, this was accompanied by a decrease in Na
Identifiants
pubmed: 38326681
doi: 10.1007/s11356-024-32283-4
pii: 10.1007/s11356-024-32283-4
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024. The Author(s).
Références
Abdel-Salam Omar ME, Galal AF, Hassanane MM, Salem LM, Nada SA, Morsy FA (2018a) Grape seed extract alone or combined with atropine in treatment of malathi-on induced neuro- and genotoxicity. J Nanosci Nanotechnol 18:564–575. https://doi.org/10.1166/jnn.2018.13943
doi: 10.1166/jnn.2018.13943
pubmed: 29768882
Abdel-Salam Omar ME, Sleem AA, Youness ER, Morsy FA (2018b) Preventive effects of c-annabis on neurotoxic and hepatotoxic activities of malathion in rat. Asian Pac J Trop Med 11:272–279. https://doi.org/10.4103/1995-7645.231467
doi: 10.4103/1995-7645.231467
Aker WG, Hu X, Wang P, Hwang HM (2008) Comparing the relative toxicity of malathio-n and malaoxon in blue catfish Ictalurus furcatus. Environ Toxicol 23:548–554. https://doi.org/10.1002/tox.20371
doi: 10.1002/tox.20371
pubmed: 18247417
Amin M, Yousuf M, Ahmad N (2022) Effects of pesticides on total protein content of D-ifferent organs of Oreochromis niloticus (Linnaeus,1758). Pak J Zool 54:1435–1438. https://doi.org/10.17582/journal.pjz/20201118201101
doi: 10.17582/journal.pjz/20201118201101
Angel Torres M (2010) ROS in biotic interactions. Physiol Plant 138:414–429. https://doi.org/10.1111/j.1399-3054.2009.01326.x
doi: 10.1111/j.1399-3054.2009.01326.x
Bhardwaj JK, Saraf P (2016) Granulosa cell apoptosis by impairing antioxidant defense system and cellular integrity in Caprine Antral follicles post malathion exposure. Environ Toxicol 31:1944–1954. https://doi.org/10.1002/tox.22195
doi: 10.1002/tox.22195
pubmed: 26420608
Bhardwaj JK, Saraf P, Kumari P, Mittal M, Kumar V (2018) N-Acetyl-cysteine mediated i-nhibition of spermatogonial cells apoptosis against malathion exposure in testicular tissue. J Biochem Mol Toxicol 32:e22046. https://doi.org/10.1002/jbt.22046
doi: 10.1002/jbt.22046
pubmed: 29457669
Bouchelaghem S, Das S, Naorem RS, Czuni L, Papp G, Kocsis M (2022) Evaluation of total phenolic and flavonoid contents, antibacterial and antibiofilm activities of hungarian propolis ethanolic extract against Staphylococcus aureus. Molecules 27:574. https://doi.org/10.3390/molecules27020574
doi: 10.3390/molecules27020574
pubmed: 35056886
pmcid: 8782033
Chen X, Wang Y, Shen M, Yu Q, Chen Y, Huang L, Xie J (2021) The water-soluble non-starch polysaccharides from natural resources against excessive oxidative stress: a potential health-promoting effect and its mechanisms. Int J Biol Macromol 171:320–330. https://doi.org/10.1016/j.ijbiomac.2021.01.022
doi: 10.1016/j.ijbiomac.2021.01.022
pubmed: 33421468
Coremen M, Turkyilmaz IB, Us H, Us AS, Celik S, Ozel AE, Bulan OK, Yanardag R (2022) Lupeol inhibits pesticides induced hepatotoxicity via reducing oxidative stress and inflammatory markers in rats. Food Chem Toxicol 164:113068. https://doi.org/10.1016/j.fct.2022.113068
doi: 10.1016/j.fct.2022.113068
pubmed: 35483487
Cui J, Wei Y, Jiang J, Xiao S, Liu X, Zhou Z, Liu D, Wang P (2023) Bioaccumulation, metabolism and toxicological effects of chiral insecticide malathion and its metabol-ites in zebrafish (Danio rerio). Chemosphere 318:137898. https://doi.org/10.1016/j.chemosphere.2023.137898
doi: 10.1016/j.chemosphere.2023.137898
pubmed: 36702415
Dar MA, Chanwala J, Meena PR, Singh AP, Kaushik G (2022) Biodegradation of malathi-on by Micrococcus sp. strain MAGK3: kinetics and degradation fragments. Arch Microbiol 204:482. https://doi.org/10.1007/s00203-022-03106-2
doi: 10.1007/s00203-022-03106-2
pubmed: 35834020
Deng X, Zhou Y, Zheng W, Bai L, Zhou X (2018) Dissipation dynamic and final residues of oxadiargyl in paddy fields using high-performance liquid chromatography-tandem mass spectrometry coupled with modified QuEChERS method. Int J En-Viron Res Public Health 15:1680. https://doi.org/10.3390/ijerph15081680
doi: 10.3390/ijerph15081680
Esen M, Uysal M (2018) Protective effects of intravenous lipid emulsion on malathion-induced hepatotoxicity. Bratisl Med J 119:373–378. https://doi.org/10.4149/BLL_2018_069
doi: 10.4149/BLL_2018_069
Fasnacht M, Polacek N (2021) Oxidative stress in bacteria and the central dogma of molecular biology. Front Mol Biosci 8:671037. https://doi.org/10.3389/fmolb.2021.671037
doi: 10.3389/fmolb.2021.671037
pubmed: 34041267
pmcid: 8141631
Flores D, Souza V, Betancourt M, Teteltitla M, Gonzalez-Marquez H, Casas E, Bonilla E, Ramirez-Noguera P, Concepcion Gutierrez-Ruiz M, Ducolomb Y (2017) Oxidative stress as a damage mechanism in porcine cumulus-oocyte complexes exposed to m-alathion during in vitro maturation. Environ Toxicol 32:1669–1678. https://doi.org/10.1002/tox.22384
doi: 10.1002/tox.22384
pubmed: 28185390
Geed SR, Kureel MK, Shukla AK, Singh RS, Rai BN (2016) Biodegradation of malathion and evaluation of kinetic parameters using three bacterial species. Resour-Effic Te-Chnol 2:S3–S11. https://doi.org/10.1016/j.reffit.2016.09.005
doi: 10.1016/j.reffit.2016.09.005
Han P, Shen S, Guo R, Zhao D, Lin YH, Jia S, Yan R, Wu Y (2019) ROS is a factor regulating the increased polysaccharide production by light quality in the edible Cyanobacterium nostoc flagelliforme. J Agric Food Chem 67:2235–2244. https://doi.org/10.1021/acs.jafc.8b06176
doi: 10.1021/acs.jafc.8b06176
pubmed: 30724068
Hasanuzzaman M, Raihan MRH, Masud AAC, Rahman K, Nowroz F, Rahman M, Nahar K, Fujita M (2021) Regulation of reactive oxygen species and antioxidant defense in plants under salinity. Int J Mol Sci 22:9326. https://doi.org/10.3390/ijms22179326
doi: 10.3390/ijms22179326
pubmed: 34502233
pmcid: 8430727
Heidar H, Seyed Taghi Omid N, Abbasali Z (2017) Monitoring organophosphorous pesticides residues in the Shahid Rajaei Dam Reservoir, Sari. Iran Bull Environ Contam Toxicol 98:791–797. https://doi.org/10.1007/s00128-017-2080-z
doi: 10.1007/s00128-017-2080-z
pubmed: 28405693
Huang Z, He K, Song Z, Zeng G, Chen A, Yuan L, Li H, Hu L, Guo Z, Chen G (2018) Antioxidative response of Phanerochaete chrysosporium against silver nanoparticle-induced toxicity and its potential mechanism. Chemosphere 211:573–583. https://doi.org/10.1016/j.chemosphere.2018.07.192
doi: 10.1016/j.chemosphere.2018.07.192
pubmed: 30092538
Ibrahim WM, Karam MA, El-Shahat R, Adway AA (2014) Biodegradation and utilization of organophosphorus pesticide malathion by cyanobacteria. Biomed Res Int 392682. https://doi.org/10.1155/2014/392682
Ishag AESA, Abdelbagi AO, Hammad AMA, Elsheikh EAE, Elsaid OE, Hur JH, Laing MD (2016) Biodegradation of chlorpyrifos, malathion, and dimethoate by three strains of bacteria isolated from pesticide-polluted soils in Sudan. J Agr Food Chem 64:8491–8498. https://doi.org/10.1021/acs.jafc.6b03334
doi: 10.1021/acs.jafc.6b03334
Ji L, Chauhan A, Brown WT, Chauhan V (2009) Increased activities of Na
doi: 10.1016/j.lfs.2009.10.008
Jiang J, Liu H, Li Q, Gao N, Yao Y, Xu H (2015) Combined remediation of Cd-phenanthrene co-contaminated soil by Pleurotus cornucopiae and Bacillus thuringiensis FQ1 and the antioxidant responses in Pleurotus cornucopiae. Ecotox Environ Safe 120:386–393. https://doi.org/10.1016/j.ecoenv.2015.06.028
doi: 10.1016/j.ecoenv.2015.06.028
Khan S, Zaffar H, Irshad U, Ahmad R, Khan AR, Shah MM, Bilal M, Iqbal M, Naqvi T (2016) Biodegradation of malathion by Bacillus licheniformis strain Ml-1. Arch Biol Sci 68:51–59. https://doi.org/10.2298/ABS141218007K
doi: 10.2298/ABS141218007K
Kopycinska M, Lipa P, Ciesla J, Koziel M, Janczarek M (2018) Extracellular polysacchari-de protects Rhizobium leguminosarum cells against zinc stress in vitro and during symbiosis with clover. Environ Microbiol Rep 10:355–368. https://doi.org/10.1111/1758-2229.12646
doi: 10.1111/1758-2229.12646
pubmed: 29633524
Krstić D, Çolović M, Kralj MB, Trebše P, Krinulović K, Vasić V (2008) The influence of malathion and its decomposition products on free and immobilized acetylcholinesterase1. Russ J Phys Chem 82:663–668. https://doi.org/10.1134/S0036024408040274
doi: 10.1134/S0036024408040274
Kumar S, Kaushik G, Dar MA, Nimesh S, López-chuken UJ, Villarreal-chiu JF (2018) Mi-crobial degradation of organophosphate pesticides: a review. Pedosphere 28:190–208. https://doi.org/10.1016/S1002-0160(18)60017-7
doi: 10.1016/S1002-0160(18)60017-7
Li Q, Huang Y, Du Y, Feng X, Dong J, Zhu J, Li Y, Zhang G, Ding D (2023) Biodecol-orization of cationic red X-GRL by immobilized Shewanella oneidensis MR-1. Water Air Soil Pollut 234:279. https://doi.org/10.1007/s11270-023-06295-8
doi: 10.1007/s11270-023-06295-8
Li Q, Peprah B, Dong J, Hu R, Shen X, Zhang XF, Liu ZY, Jiang XP (2021) Neutral re-d mediated reductive decolorization of metal complex azo dye by Shewanella oneidensis MR-1. Pol J Environ Stud 30:5105–5116. https://doi.org/10.15244/pjoes/133719
doi: 10.15244/pjoes/133719
Liu L, Zhu B, Gong YX, Liu GL, Wang GX (2015) Neurotoxic effect of triazophos on goldfish (Carassius auratus) and tissue specific antioxidant responses. Ecotox Environ Safe 116:68–75. https://doi.org/10.1016/j.ecoenv.2015.03.001
doi: 10.1016/j.ecoenv.2015.03.001
Liu Y, Climent V, Berna A, Miguel Feliu J (2011) Effect of temperature on the catalytic ability of electrochemically active biofilm as anode catalyst in microbial fuel cells. Electroanalysis 23:387–394. https://doi.org/10.1002/elan.201000499
doi: 10.1002/elan.201000499
Meng LW, Peng ML, Chen ML, Yuan GR, Zheng LS, Bai WJ, Guy S, Wang JJ (2020) A glutathione S-transferase (BdGSTd9) participates in malathion resistance via directly depleting malathion and its toxic oxide malaoxon in Bactrocera dorsalis (Hendel). Pest Manag Sci 76:2557–2568. https://doi.org/10.1002/ps.5810
doi: 10.1002/ps.5810
pubmed: 32128980
Meyer-Cifuentes IE, Werner J, Jehmlich N, Will SE, Neumann-Schaal M, Oeztuerk B (2020) Synergistic biodegradation of aromatic-aliphatic copolyester plastic by a marine microbial consortium. Nat Commun 11:5790. https://doi.org/10.1038/s41467-020-19583-2
doi: 10.1038/s41467-020-19583-2
pubmed: 33188179
pmcid: 7666164
Nanda M, Kumar V, Fatima N, Pruthi V, Verma M, Chauhan PK, Vlaskin MS, Grigorenko AV (2019) Detoxification mechanism of organophosphorus pesticide via carboxyl-estrase pathway that triggers de novo TAG biosynthesis in oleaginous microalgae. Aquat Toxicol 209:49–55. https://doi.org/10.1016/j.aquatox.2019.01.019
doi: 10.1016/j.aquatox.2019.01.019
pubmed: 30711855
Nasirin C, Najm MAA, Chen TC, Dhamija A, Lionardo A, Bokov DO, Naserabad SS (2023) The protective effects of quercetin on the physiological responses in malathion-exposed common carp. Cyprinus Carpio Trop Anim Health Prod 55:22. https://doi.org/10.1007/s11250-022-03429-8
doi: 10.1007/s11250-022-03429-8
Ningthoujam M, Habib K, Bano F, Zutshi S, Fatma T (2013) Exogenous osmolytes supper-sses the toxic effects of malathion on Anabaena variabilis. Ecotoxicol Environ Saf 94:21–27. https://doi.org/10.1016/j.ecoenv.2013.04.022
doi: 10.1016/j.ecoenv.2013.04.022
pubmed: 23706601
Ojha A, Yaduvanshi SK, Srivastava N (2011) Effect of combined exposure of commonly used organophosphate pesticides on lipid peroxidation and antioxidant enzymes in r-at tissues. Pest Biochem Physiol 99:148–156. https://doi.org/10.1016/j.pestbp.2010.11.011
doi: 10.1016/j.pestbp.2010.11.011
Olakkaran S, Kizhakke Purayil A, Antony A, Mallikarjunaiah S, Hunasanahally Puttaswamygowda G (2020) Oxidative stress-mediated genotoxicity of malathion in human lymphocytes. Mutat Res Gen Tox En 849:503138. https://doi.org/10.1016/j.mrgentox.2020.503138
doi: 10.1016/j.mrgentox.2020.503138
Osman KA, El-Din EME, Ahmed NS, El-Seedy AS (2021) Effect of N-acetylcysteine on attenuation of chlropyrifos and its methyl analogue toxicity in male rats. Toxicology 461:152904. https://doi.org/10.1016/j.tox.2021.152904
doi: 10.1016/j.tox.2021.152904
pubmed: 34425170
Pattarachotanant N, Tencomnao T (2020) Citrus hystrix extracts protect human neuronal cells against high glucose-induced senescence. Pharmaceuticals 13:283. https://doi.org/10.3390/ph13100283
doi: 10.3390/ph13100283
pubmed: 33007805
pmcid: 7600454
Poopal RK, Ramesh M, Dinesh B (2013) Short-term mercury exposure on Na
doi: 10.1016/j.jtemb.2012.06.002
pubmed: 22944584
Rebechi D, Palacio-Cortés AM, Richardi VS, Beltrão T, Vicentini M, Grassi MT, da Silva SB, Alessandre T, Hasenbein S, Connon R, Navarro-Silva MA (2021) Molecular and biochemical evaluation of effects of malathion, phenanthrene and cadmium on Chironomus sancticaroli (Diptera: Chironomidae) larvae. Ecotox Environ Safe 211:111953. https://doi.org/10.1016/j.ecoenv.2021.111953
doi: 10.1016/j.ecoenv.2021.111953
Reddy MV, Yajima Y, Choi D, Chang YC (2017) Biodegradation of toxic organic compounds using a newly isolated Bacillus sp. CYR2. Biotechnol Bioproc E 22:339–346. https://doi.org/10.1007/s12257-017-0117-0
doi: 10.1007/s12257-017-0117-0
Ren W, Chang H, Teng Y (2016) Sulfonated graphene-induced hormesis is mediated through oxidative stress in the roots of maize seedlings. Sci Total Environ 572:926–934. https://doi.org/10.1016/j.scitotenv.2016.07.214
doi: 10.1016/j.scitotenv.2016.07.214
pubmed: 27503631
Shahid M, Khan MS, Syed A, Marraiki N, Elgorban AM (2021) Mesorhizobium ciceri as biological tool for improving physiological, biochemical and antioxidant state of Cicer aritienum (L.) under fungicide stress. Sci Rep 11:9655. https://doi.org/10.1038/s41598-021-89103-9
doi: 10.1038/s41598-021-89103-9
pubmed: 33958646
pmcid: 8102606
Shi S, Tang D, Liu Y (2009) Effects of an algicidal bacterium Pseudomonas mendocina on the growth and antioxidant system of Aphanizomenon flosaquae. Curr Microbiol 59:107–112. https://doi.org/10.1007/s00284-009-9404-0
doi: 10.1007/s00284-009-9404-0
pubmed: 19365689
Silva-Madera RJ, Salazar-Flores J, Peregrina-Lucano AA, Mendoza-Michel J, Ceja-Galvez HR, Rojas-Bravo D, Reyna-Villela MZ, Torres-Sanchez ED (2021) Pesticide contamination in drinking and surface water in the Cienega, Jalisco. Mexico Water Ai-r Soil Pollut 232:43. https://doi.org/10.1007/s11270-021-04990-y
doi: 10.1007/s11270-021-04990-y
Springthorpe SK, Dundas CM, Keitz BK (2019) Microbial reduction of metal-organic frameworks enables synergistic chromium removal. Nat Commun 10:5212. https://doi.org/10.1038/s41467-019-13219-w
doi: 10.1038/s41467-019-13219-w
pubmed: 31740677
pmcid: 6861306
Tang S, Yin H, Zhou S, Chen S, Peng H, Liu Z, Dang Z (2016) Simultaneous Cr (VI) removal and 2,2’,4,4’-tetrabromodiphenyl ether (BDE-47) biodegradation by Pseudomonas aeruginosa in liquid medium. Chemosphere 150:24–32. https://doi.org/10.1016/j.chemosphere.2016.02.010
doi: 10.1016/j.chemosphere.2016.02.010
pubmed: 26891353
Tao MT, Bian ZQ, Zhang J, Wang T, Shen HY (2020) Quantitative evaluation and the toxicity mechanism of synergism within three organophosphorus pesticide mixtures to Chlorella pyrenoidosa. Environ Sci: Processes Impacts 22:2095–2103. https://doi.org/10.1039/D0EM00262C
doi: 10.1039/D0EM00262C
Tian J, Xu Q, Wang X, Zhang X, Chen X, Rui X, Zhang Q, Dong M, Li W (2023) Protective effects and mechanism of Paecilomyces cicadae TJJ1213 intracellular polysaccharide against H
doi: 10.1111/cbdd.14253
pubmed: 37072242
Tiwari B, Singh S, Chakraborty S, Verma E, Mishra AK (2017) Sequential role of biosorption and biodegradation in rapid removal degradation and utilization of methyl parathion as a phosphate source by a new cyanobacterial isolate Scytonema sp. BHUS-5. Int J Phytorem 19:884–893. https://doi.org/10.1080/15226514.2017.1303807
doi: 10.1080/15226514.2017.1303807
Tudi M, Daniel Ruan H, Wang L, Lyu J, Sadler R, Connell D, Chu C, Phung DT (2021) Agriculture development, pesticide application and its impact on the environment. Int J Environ Res Public Health 18:1112. https://doi.org/10.3390/ijerph18031112
doi: 10.3390/ijerph18031112
pubmed: 33513796
pmcid: 7908628
Ullah S, Li Z, Hasan Z, Khan SU, Fahad S (2018) Malathion induced oxidative stress leads to histopathological and biochemical toxicity in the liver of rohu (Labeo rohita, Hamilton) at acute concentration. Ecotox Environ Safe 161:270–280. https://doi.org/10.1016/j.ecoenv.2018.06.002
doi: 10.1016/j.ecoenv.2018.06.002
Uysal M, Karaman S (2018) In vivo effects of intravenous lipid emulsion on lung tissue in an experimental model of acute malathion intoxication. Toxicol Ind Health 34:110–118. https://doi.org/10.1177/0748233717748080
doi: 10.1177/0748233717748080
pubmed: 29415640
Vasseghian Y, Almomani F, Le VT, Moradi M, Dragoi EN (2022) Decontamination of toxic malathion pesticide in aqueous solutions by Fenton-based processes: degradation pathway, toxicity assessment and health risk assessment. J Hazard Mater 423:127016. https://doi.org/10.1016/j.jhazmat.2021.127016
doi: 10.1016/j.jhazmat.2021.127016
pubmed: 34474364
Venkatesan R, Park YU, Ji E, Yeo EJ, Kim SY (2017) Malathion increases apoptotic cell death by inducing lysosomal membrane permeabilization in N2a neuroblastoma cells: a model for neurodegeneration in Alzheimer’s disease. Cell Death Discov 3:17007. https://doi.org/10.1038/cddiscovery.2017.7
doi: 10.1038/cddiscovery.2017.7
pubmed: 28487766
pmcid: 5402539
Wan F, Shi M, Gao H (2017) Loss of OxyR reduces efficacy of oxygen respiration in Shewanella oneidensis. Sci Rep 7:42609. https://doi.org/10.1038/srep42609
doi: 10.1038/srep42609
pubmed: 28195212
pmcid: 5307378
Wang J, Teng Y, Zhai Y, Yue W, Pan Z (2022) Spatiotemporal distribution and risk assessment of organophosphorus pesticides in surface water and groundwater on the North China Plain. China Environ Res 204:112310. https://doi.org/10.1016/j.envres.2021.112310
doi: 10.1016/j.envres.2021.112310
pubmed: 34762928
Wang YH, Mu WJ, Sun XL, Fan YW, Liu Y (2020) Physiological response and removal ability of freshwater diatom Nitzschia palea to two organophosphorus pesticides. Chem Ecol 36:881–902. https://doi.org/10.1080/02757540.2020.1784883
doi: 10.1080/02757540.2020.1784883
Xiao X, Xu CC, Wu YM, Cai PJ, Li WW, Du DL, Yu HQ (2012) Biodecolorization of Naphthol Green B dye by Shewanella oneidensis MR-1 under anaerobic conditions. Bioresour Technol 110:86–90. https://doi.org/10.1016/j.biortech.2012.01.099
doi: 10.1016/j.biortech.2012.01.099
pubmed: 22349191
Xiong J, Tian L, Qiu Y, Sun D, Zhang H, Wu M, Wang J (2018) Evaluation on the thyroid disrupting mechanism of malathion in Fischer rat thyroid follicular cell line FRTL-5. Drug Chem Toxicol 41:501–508. https://doi.org/10.1080/01480545.2017.1397162
doi: 10.1080/01480545.2017.1397162
pubmed: 29143548
Yang W, Yingjun W, Jinge D, Zhanghong W, Qinglian W (2016) Effects of yttrium under lead stress on growth and physiological characteristics of Microcystis aeruginosa. J Rare Earths 34:747–756. https://doi.org/10.1016/S1002-0721(16)60089-3
doi: 10.1016/S1002-0721(16)60089-3
Zhang L, Wu L, Mi Y, Si Y (2019) Silver Nanoparticles Induced Cell Apoptosis, Membrane damage of Azotobacter vinelandii and Nitrosomonas europaea via generation of reactive oxygen species. Bull Environ Contam Toxicol 103:181–186. https://doi.org/10.1007/s00128-019-02622-0
doi: 10.1007/s00128-019-02622-0
pubmed: 31049596
Zhao C, Li Y, Li X, Huang H, Zheng G, Chen Y (2022) Biological removal of sulfamethoxazole enhanced by S. oneidensis MR-1 via promoting NADH generation and electron transfer and consumption. J Hazard Mater 426:127839. https://doi.org/10.1016/j.jhazmat.2021.127839
doi: 10.1016/j.jhazmat.2021.127839
pubmed: 34838361
Zhao F, Wang B, Zhang XN, Tian H, Wang W, Ru SG (2015) Induction of DNA base damage and strand breaks in peripheral erythrocytes and the underlying mechanism in goldfish (Carassius auratus) exposed to monocrotophos. Fish Physiol Biochem 41:613–624. https://doi.org/10.1007/s10695-015-0032-2
doi: 10.1007/s10695-015-0032-2
pubmed: 25666866
Zhao S, Xu W, Zhang W, Wu H, Guang C, Mu W (2021) Overview of a bioremediation tool: organophosphorus hydrolase and its significant application in the food, environmental, and therapy fields. Appl Microbiol Biotechnol 105:8241–8253. https://doi.org/10.1007/s00253-021-11633-z
doi: 10.1007/s00253-021-11633-z
pubmed: 34665276
Zou L, Huang Y, Long Z, Qiao Y (2018) On-going applications of Shewanella species in microbial electrochemical system for bioenergy, bioremediation and biosensing. World J Microbiol Biotechnol 35:9. https://doi.org/10.1007/s11274-018-2576-7
doi: 10.1007/s11274-018-2576-7
pubmed: 30569420