Abstract
Methyl parathion (MP) is a highly toxic organophosphorus pesticide associated with water, soil, and air pollution events. The identification and characterization of microorganisms capable of biodegrading pollutants are an important environmental task for bioremediation of pesticide impacted sites. The strain Burkholderia cenocepacia CEIB S5-2 is a bacterium capable of efficiently hydrolyzing MP and biodegrade p-nitrophenol (PNP), the main MP hydrolysis product. Due to the high PNP toxicity over microbial living forms, the reports on bacterial PNP biodegradation are scarce. According to the genomic data, the MP- and PNP-degrading ability observed in B. cenocepacia CEIB S5-2 is related to the presence of the methyl parathion-degrading gene (mpd) and the gene cluster pnpABA’E1E2FDC, which include the genes implicated in the PNP degradation. In this work, the transcriptomic analysis of the strain in the presence of MP revealed the differential expression of 257 genes, including all genes implicated in the PNP degradation, as well as a set of genes related to the sensing of environmental changes, the response to stress, and the degradation of aromatic compounds, such as translational regulators, membrane transporters, efflux pumps, and oxidative stress response genes. These findings suggest that these genes play an important role in the defense against toxic effects derived from the MP and PNP exposure. Therefore, B. cenocepacia CEIB S5-2 has a great potential for application in pesticide bioremediation approaches due to its biodegradation capabilities and the differential expression of genes for resistance to MP and PNP.
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Genomic data are available at NCBI with the following BioProject accession PRJNA 301637.
References
Akama H, Kanemaki M, Yoshimura M, Tsukihara T, Kashiwagi T, Yoneyama H, Narita SI, Nakegawa A, Nakae T (2004) Crystal structure of the drug discharge outer membrane protein, OprM, of Pseudomonas aeruginosa dual modes of membrane anchoring and occluded cavity end. J Biol Chem 279(51):52816–52819. https://doi.org/10.1074/jbc.C400445200
Bhatt P, Zhou X, Huang Y, Zhang W, Chen S (2021) Characterization of the role of esterases in the biodegradation of organophosphate, carbamate, and pyrethroid pesticides. J Hazard Mater 411(5):125026
Blanco P, Hernando-Amado S, Reales-Calderon JA, Corona F, Lira F, Alcalde-Rico M, Bernardini A, Sanchez MB, Martinez JL (2016) Bacterial multidrug efflux pumps: much more than antibiotic resistance determinants. Microorganisms 4(1):14. https://doi.org/10.3390/microorganisms4010014
Bogomolnaya LM, Andrews KD, Talamantes M, Maple A, Ragoza Y, Vazquez-Torres A, Andrews-Polymenis H (2013) The ABC-type efflux pump MacAB protects Salmonella enterica serovar typhimurium from oxidative stress. MBio 4(6):e00630–e00613. https://doi.org/10.1128/mBio.00630-13
Bryk R, Lima CD, Erdjument-Bromage H, Tempst P, Nathan C (2002) Metabolic enzymes of mycobacteria linked to antioxidant defense by a thioredoxin-like protein. Science 295(5557):1073–1077. https://doi.org/10.1126/science.1067798
Capra EJ, Laub MT (2012) Evolution of two-component signal transduction systems. Annu Rev Microbiol 66:325–347. https://doi.org/10.1146/annurev-micro-092611-150039
Castrejón-Godínez ML, Ortiz-Hernández ML, Salazar E, Encarnación S, Mussali-Galante P, Tovar-Sánchez E, Sánchez-Salinas E, Rodríguez A (2019) Transcriptional analysis reveals the metabolic state of Burkholderia zhejiangensis CEIB S4-3 during methyl parathion degradation. PeerJ 7:e6822. https://doi.org/10.7717/peerj.6822
Chakka D, Gudla R, Madikonda AK, Pandeeti EVP, Parthasarathy S, Nandavaram A, Siddavattam D (2015) The organophosphate degradation (opd) Island-borne esterase induced metabolic diversion in Escherichia coli and its influence on p-Nitrophenol degradation. J Biol Chem 290(50):29920–29930. https://doi.org/10.1074/jbc.M115.661249
Chen J, Xie J (2011) Role and regulation of bacterial LuxR-like regulators. J Cell Biochem 112(10):2694–2702. https://doi.org/10.1002/jcb.23219
Chen Q, Tu H, Luo X, Zhang B, Huang F, Li Z, Wang J, Shen W, Wu J, Cui Z (2016) The regulation of para-nitrophenol degradation in Pseudomonas putida DLL-E4. PLoS One 11(5):e0155485. https://doi.org/10.1371/journal.pone.0155485
Colclough AL, Scadden J, Blair JMA (2019) TetR-family transcription factors in Gram-negative bacteria: conservation, variation and implications for efflux-mediated antimicrobial resistance. BMC Genomics 20(1):731. https://doi.org/10.1186/s12864-019-6075-5
Cuthbertson L, Nodwell JR (2013) The TetR family of regulators. Microbiol Mol Biol Rev 77(3):440–475. https://doi.org/10.1128/MMBR.00018-13
Dorneles AL, de Souza RA, Blochtein B (2017) Toxicity of organophosphorus pesticides to the stingless bees Scaptotrigona bipunctata and Tetragonisca fiebrigi. Apidologie 48(5):612–620. https://doi.org/10.1007/s13592-017-0502-x
Fernández-López MG, Popoca-Ursino C, Sánchez-Salinas E, Tinoco-Valencia R, Folch-Mallol JL, Dantán-González E, Ortiz-Hernández ML (2017) Enhancing methyl parathion degradation by the immobilization of Burkholderia sp. isolated from agricultural soils. MicrobiologyOpen 6:e507. https://doi.org/10.1002/mbo3.507
Fishman A, Tao Y, Bentley WE, Wood TK (2004) Protein engineering of toluene 4-monooxygenase of Pseudomonas mendocina KR1 for synthesizing 4-nitrocatechol from nitrobenzene. Biotechnol Bioeng 87(6):779–790. https://doi.org/10.1002/bit.20185
Fosu-Mensah BY, Okoffo ED, Darko G, Gordon C (2016) Organophosphorus pesticide residues in soils and drinking water sources from cocoa producing areas in Ghana. Environ Syst Res 5(1):1–12. https://doi.org/10.1186/s40068-016-0063-4
Galperin MY, Makarova KS, Wolf YI, Koonin EV (2014) Expanded microbial genome coverage and improved protein family annotation in the COG database. Nucleic Acids Res 43(D1):D261–D269. https://doi.org/10.1093/nar/gku1223
Haigler BE, Gibson DT (1990) Purification and properties of NADH-ferredoxinNAP reductase, a component of naphthalene dioxygenase from Pseudomonas sp. strain NCIB 9816. J Bacteriol 172(1):457–464. https://doi.org/10.1128/jb.172.1.457-464.1990
Hammer Ø, Harper DA, Ryan PD (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electron 4(1):1–9
Hernández-Mendoza A, Martínez-Ocampo F, Lozano-Aguirre Beltrán LF, Popoca-Ursino EC, Ortiz-Hernández L, Sánchez-Salinas E, Dantán-González E (2014) Draft genome sequence of the organophosphorus compound-degrading Burkholderia zhejiangensis strain CEIB S4-3. Genome Announc 2(6):e01323–14. https://doi.org/10.1128/genomeA.01323-14
Horne I, Sutherland TD, Oakeshott JG, Russell RJ (2002) Cloning and expression of the phosphotriesterase gene hocA from Pseudomonas monteilii C11bbThe GenBank accession number for the hocA gene is AF469117. Microbiology 148(9):2687–2695. https://doi.org/10.1099/00221287-148-9-2687
Huang Y, Lemieux MJ, Song J, Auer M, Wang DN (2003) Structure and mechanism of the glycerol-3-phosphate transporter from Escherichia coli. Science. 301(5633):616–620. https://doi.org/10.1126/science.1087619
Jain RK, Dreisbach JH, Spain JC (1994) Biodegradation of p-nitrophenol via 1, 2, 4-benzenetriol by an Arthrobacter sp. Appl Environ Microbiol 60(8):3030–3032
Jiang D, Zhao Y, Wang X, Fan J, Heng J, Liu X, Feng W, Kang X, Huang B, Liu J, Zhang XC (2013) Structure of the YajR transporter suggests a transport mechanism based on the conserved motif A. Proc Natl Acad Sci 110(36):14664–14669. https://doi.org/10.1073/pnas.1308127110
Jokanović M (2018) Neurotoxic effects of organophosphorus pesticides and possible association with neurodegenerative diseases in man: a review. Toxicology 410:125–131. https://doi.org/10.1016/j.tox.2018.09.009
Kadiyala V, Smets BF, Chandran K, Spain JC (1998) High affinity p-nitrophenol oxidation by Bacillus sphaericus JS905. FEMS Microbiol Lett 166(1):115–120. https://doi.org/10.1111/j.1574-6968.1998.tb13191.x
Karasali H, Maragou N (2016) Pesticides and herbicides: types of pesticide. Encycl Food Health:319–325. https://doi.org/10.1016/B978-0-12-384947-2.00535-3
Kitagawa W, Kimura N, Kamagata Y (2004) A novel p-nitrophenol degradation gene cluster from a gram-positive bacterium, Rhodococcus opacus SAO101. J Bacteriol 186(15):4894–4902. https://doi.org/10.1128/JB.186.15.4894-4902.2004
Koh S, Hwang J, Guchhait K, Lee EG, Kim SY, Kim S, Lee S, Chung JM, Jung HS, Lee SJ, Ryu CM, Lee SG, Oh TK, Kwon O, Kim MH (2016) Molecular insights into toluene sensing in the TodS/TodT signal transduction system. J Biol Chem 291(16):8575–8590. https://doi.org/10.1074/jbc.M116.718841
Kulkarni M, Chaudhari A (2006) Biodegradation of p-nitrophenol by P. putida. Bioresour Technol 97(8):982–988. https://doi.org/10.1016/j.biortech.2005.04.036
Kumar S, Vikram S, Raghava GPS (2012) Genome sequence of the nitroaromatic compound-degrading bacterium Burkholderia sp. strain SJ98. Genome Announc 194(12):3286. https://doi.org/10.1128/JB.00497-12
Kvint K, Nachin L, Diez A, Nyström T (2003) The bacterial universal stress protein: function and regulation. Curr Opin Microbiol 6(2):140–145. https://doi.org/10.1016/S1369-5274(03)00025-0
Lau PC, Wang Y, Patel A, Labbé D, Bergeron H, Brousseau R, Konishi Y, Rawlings M (1997) A bacterial basic region leucine zipper histidine kinase regulating toluene degradation. Proc Natl Acad Sci 94(4):1453–1458. https://doi.org/10.1073/pnas.94.4.1453
Le Minh PN, de Cima S, Bervoets I, Maes D, Rubio V, Charlier D (2015) Ligand binding specificity of RutR, a member of the TetR family of transcription regulators in Escherichia coli. FEBS Open Biol 5:76–84. https://doi.org/10.1016/j.fob.2015.01.002
Li Z, Xiang Z, Zeng J, Li Y, Li J (2019) A GntR family transcription factor in Streptococcus mutans regulates biofilm formation and expression of multiple sugar transporter genes. Front Microbiol 9:3224. https://doi.org/10.3389/fmicb.2018.03224
Lim JS, Choi BS, Choi AY, Kim KD, Kim DI, Choi IY, Ka JO (2012) Complete genome sequence of the fenitrothion-degrading Burkholderia sp. strain YI23. J Bacteriol 194:896–811. https://doi.org/10.1128/JB.06479-11
Liu S, Su T, Zhang C, Zhang WM, Zhu D, Su J, Zhou NY, Xu S (2015) Crystal structure of PnpCD, a two-subunit hydroquinone 1, 2-dioxygenase, reveals a novel structural class of Fe2+-dependent dioxygenases. J Biol Chem 290(40):24547–24560. https://doi.org/10.1074/jbc.M115.673558
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25(4):402–408. https://doi.org/10.1006/meth.2001.1262
Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15(12):550. https://doi.org/10.1186/s13059-014-0550-8
Lu W, Li L, Chen M, Zhou Z, Zhang W, Ping S, Yan Y, Wang J, Lin M (2013) Genome-wide transcriptional responses of Escherichia coli to glyphosate, a potent inhibitor of the shikimate pathway enzyme 5-enolpyruvylshikimate-3-phosphate synthase. Mol BioSyst 9(3):522–530. https://doi.org/10.1039/C2MB25374G
Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J 17(1):10–12. https://doi.org/10.14806/ej.17.1.200
Martin VJ, Mohn WW (1999) A novel aromatic-ring-hydroxylating dioxygenase from the diterpenoid-degrading bacterium Pseudomonas abietaniphila BKME-9. J Bacteriol 181(9):2675–2682. https://doi.org/10.1128/JB.181.9.2675-2682.1999
Martínez-Ocampo F, López MGF, Beltrán LFLA, Popoca-Ursino EC, Ortiz-Hernández ML, Sánchez-Salinas E, Ramos-Quintana F, Villalobos-López MA, Dantán-González E (2016) Draft genome sequence of Burkholderia cenocepacia strain CEIB S5-2, a methyl parathion-and p-Nitrophenol-degrading bacterium, isolated from agricultural soils in Morelos, Mexico. Genome Announc 4(2):e00220–e00216. https://doi.org/10.1128/genomeA.00220-16
Megharaj M, Pearson HW, Venkateswarlu K (1991) Toxicity of p-aminophenol and p-nitrophenol to Chlorella vulgaris and two species of Nostoc isolated from soil. Pestic Biochem Physiol 40(3):266–273. https://doi.org/10.1016/0048-3575(91)90098-7
Min J, Wang B, Hu X (2017) Effect of inoculation of Burkholderia sp. strain SJ98 on bacterial community dynamics and para-nitrophenol, 3-methyl-4-nitrophenol, and 2-chloro-4-nitrophenol degradation in soil. Sci Rep 7(1):1–9. https://doi.org/10.1038/s41598-017-06436-0
Mulbry WW, Karns JS (1989) Parathion hydrolase specified by the Flavobacterium opd gene: relationship between the gene and protein. J Bacteriol 171(12):6740–6746. https://doi.org/10.1128/jb.171.12.6740-6746.1989
Mulla SI, Ameen F, Talwar MP, Eqani SAMAS, Bharagava RN, Saxena G, Tallur PN, Ninnekar HZ (2020) Organophosphate pesticides: impact on environment, toxicity, and their degradation. In: Saxena G, Bharagava RN (eds) Bioremediation of industrial waste for environmental safety. Springer, Singapore, pp 265–290. https://doi.org/10.1007/978-981-13-1891-7_13
Nachin L, Nannmark U, Nyström T (2005) Differential roles of the universal stress proteins of Escherichia coli in oxidative stress resistance, adhesion, and motility. J Bacteriol 187(18):6265–6272. https://doi.org/10.1128/JB.187.18.6265-6272.2005
Nicolopoulou-Stamati P, Maipas S, Kotampasi C, Stamatis P, Hens L (2016) Chemical pesticides and human health: the urgent need for a new concept in agriculture. Front Public Health 4:148. https://doi.org/10.3389/fpubh.2016.00148
Nikaido E, Shirosaka I, Yamaguchi A, Nishino K (2011) Regulation of the AcrAB multidrug efflux pump in Salmonella enterica serovar Typhimurium in response to indole and paraquat. Microbiology 157(3):648–655. https://doi.org/10.1099/mic.0.045757-0
Nunn CM, Djordjevic S, Hillas PJ, Nishida CR, de Montellano PRO (2002) The crystal structure of Mycobacterium tuberculosis alkylhydroperoxidase AhpD, a potential target for antitubercular drug design. J Biol Chem 277(22):20033–20040. https://doi.org/10.1074/jbc.M200864200
Ogata H, Goto S, Sato K, Fujibuchi W, Bono H, Kanehisa M (1999) KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res 27(1):29–34. https://doi.org/10.1093/nar/27.1.29
Okoli UA, Nubila NI, Okafor MT (2017) Organophosphorus pesticide: an environmental pollutant perspective. J Chem Pharm Res 9(9):126–130
Osman D, Cavet JS (2010) Bacterial metal-sensing proteins exemplified by ArsR–SmtB family repressors. Nat Prod Rep 27(5):668–680. https://doi.org/10.1039/B906682A
Paget MS, Helmann JD (2003) The σ 70 family of sigma factors. Genome Biol 4(1):203. https://doi.org/10.1186/gb-2003-4-1-203
Pailan S, Sengupta K, Saha P (2020) Microbial metabolism of organophosphates: key for developing smart bioremediation process of next generation. In: Arora PK (ed) Microbial Technology for Health and Environment. Springer, Singapore, pp 361–410. https://doi.org/10.1007/978-981-15-2679-4_14
Pakala SB, Gorla P, Pinjari AB, Krovidi RK, Baru R, Yanamandra M, Merrick M, Siddavattam D (2007) Biodegradation of methyl parathion and p-nitrophenol: evidence for the presence of a p-nitrophenol 2-hydroxylase in a Gram-negative Serratia sp. strain DS001. Appl Microbiol Biotechnol 73(6):1452–1462. https://doi.org/10.1007/s00253-006-0595-z
Phan G, Benabdelhak H, Lascombe MB, Benas P, Rety S, Picard M, Ducruix A, Etchebest C, Broutin I (2010) Structural and dynamical insights into the opening mechanism of P. aeruginosa OprM channel. Structure 18(4):507–517. https://doi.org/10.1016/j.str.2010.01.018
Poirier L, Jacquet P, Plener L, Masson P, Daudé D, Chabrière E (2018) Organophosphorus poisoning in animals and enzymatic antidotes. Environ Sci Pollut Res. https://doi.org/10.1007/s11356-018-2465-5
Popoca-Ursino EC, Martínez-Ocampo F, Dantán-González E, Sánchez-Salinas E, Ortiz-Hernández ML (2017) Characterization of methyl parathion degradation by a Burkholderia zhejiangensis strain, CEIB S4-3, isolated from agricultural soils. Biodegradation 28(5-6):351–367. https://doi.org/10.1007/s10532-017-9801-1
Schroeder A, Mueller O, Stocker S, Salowsky R, Leiber M, Gassmann M, Lightfoot S, Menzel W, Granzow M, Ragg T (2006) The RIN: an RNA integrity number for assigning integrity values to RNA measurements. BMC Mol Biol 7(1):3. https://doi.org/10.1186/1471-2199-7-3
Sharma RK, Singh P, Setia A, Sharma AK (2020) Insecticides and ovarian functions. Environ Mol Mutagen 61(3):369–392. https://doi.org/10.1002/em.22355
Shen W, Liu W, Zhang J, Tao J, Deng H, Cao H, Cui Z (2010) Cloning and characterization of a gene cluster involved in the catabolism of p-nitrophenol from Pseudomonas putida DLL-E4. Bioresour Technol 101(19):7516–7522. https://doi.org/10.1016/j.biortech.2010.04.052
Siddavattam D, Khajamohiddin S, Manavathi B, Pakala SB, Merrick M (2003) Transposon-like organization of the plasmid-borne organophosphate degradation (opd) gene cluster found in Flavobacterium sp. Appl Environ Microbiol 69(5):2533–2539. https://doi.org/10.1128/AEM.69.5.2533-2539.2003
Siddiqa A, Islam MJ, Rahman MS, Uddin MN, Fancy R (2016) Assessing toxicity of organophosphorus insecticide on local fish species of Bangladesh. Int J Fish Aquat Stud 4:670–676
Spain JC, Gibson DT (1991) Pathway for biodegradation of p-nitrophenol in a Moraxella sp. Appl Environ Microbiol 57(3):812–819
Stanley J, Preetha G (2016) Pesticide toxicity to microorganisms: exposure, toxicity and risk assessment methodologies. In: Pesticide toxicity to non-target organisms. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-7752-0_6
Subashchandrabose SR, Megharaj M, Venkateswarlu K, Naidu R (2012) p-Nitrophenol toxicity to and its removal by three select soil isolates of microalgae: the role of antioxidants. Environ Toxicol Chem 31(9):1980–1988. https://doi.org/10.1002/etc.1931
Symmons MF, Bokma E, Koronakis E, Hughes C, Koronakis V (2009) The assembled structure of a complete tripartite bacterial multidrug efflux pump. Proc Natl Acad Sci 106(17):7173–7178. https://doi.org/10.1073/pnas.0900693106
Takeo M, Murakami M, Niihara S, Yamamoto K, Nishimura M, Kato DI, Negoro S (2008) Mechanism of 4-nitrophenol oxidation in Rhodococcus sp. strain PN1: characterization of the two-component 4-nitrophenol hydroxylase and regulation of its expression. J Bacteriol 190(22):7367–7374. https://doi.org/10.1128/JB.00742-08
Takeshita K, Shibata TF, Nikoh N, Nishiyama T, Hasebe M, Fukatsu T, Shigenobu S, Kikuchi Y (2014) Whole-genome sequence of Burkholderia sp. strain RPE67, a bacterial gut symbiont of the bean bug Riptortus pedestris. Genome Announc 2(3):e00556–e00514. https://doi.org/10.1128/genomeA.00556-14
Thorvaldsdóttir H, Robinson JT, Mesirov JP (2013) Integrative genomics viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform 14(2):178–192. https://doi.org/10.1093/bib/bbs017
Tiwari B, Verma E, Chakraborty S, Srivastava AK, Mishra AK (2018) Tolerance strategies in cyanobacterium Fischerella sp. under pesticide stress and possible role of a carbohydrate-binding protein in the metabolism of methyl parathion (MP). Int Biodeterior Biodegradation 127:217–226. https://doi.org/10.1016/j.ibiod.2017.11.025
Upadhayay J, Rana M, Juyal V, Bisht SS, Joshi R (2020) Impact of pesticide exposure and associated health effects. In: Srivastava PK, Singh VP, Singh A, Tripathi DK, Singh S, Prasad SM, Chauhan DK (eds) Pesticides in crop production: physiological and biochemical action. John Wiley and Sons Ltd., Hoboken, pp 69–88. https://doi.org/10.1002/9781119432241.ch5
Urióstegui-Acosta M, Tello-Mora P, Solís-Heredia MJ, Ortega-Olvera JM, Piña-Guzmán B, Martín-Tapia D, González-Mariscal L, Quintanilla-Vega B (2020) Methyl parathion causes genetic damage in sperm and disrupts the permeability of the blood-testis barrier by an oxidant mechanism in mice. Toxicology 438:152463. https://doi.org/10.1016/j.tox.2020.152463
Vikram S, Pandey J, Bhalla N, Pandey G, Ghosh A, Khan F, Jain RK, Raghava GP (2012) Branching of the p-nitrophenol (PNP) degradation pathway in Burkholderia sp. strain SJ98: evidences from genetic characterization of PNP gene cluster. AMB Express 2(1):30. https://doi.org/10.1186/2191-0855-2-30
Vikram S, Pandey J, Kumar S, Raghava GPS (2013) Genes involved in degradation of para-nitrophenol are differentially arranged in form of non-contiguous gene clusters in Burkholderia sp. strain SJ98. PLoS One 8(12):1–13. https://doi.org/10.1371/journal.pone.0084766
Vollmer AC, Bark SJ (2018) Twenty-five years of investigating the universal stress protein: function, structure, and applications. In: Sariaslani S, Gadd GM (eds) Advances in Applied Microbiology. Academic Press, United States, pp 1–36. https://doi.org/10.1016/bs.aambs.2017.10.001
Wei Q, Liu H, Zhang JJ, Wang SH, Xiao Y, Zhou, NY (2010) Characterization of a para-nitrophenol catabolic cluster in Pseudomonas sp. strain NyZ402 and construction of an engineered strain capable of simultaneously mineralizing both para-and ortho-nitrophenols. Biodegradation 21(4):575–584. https://doi.org/10.1007/s10532-009-9325-4
Zar JH (2010) Biostatistical analysis, 5th edn. Prentice Hall, New Jersey, p 944
Zhang J, Sun Z, Li Y, Peng X, Li W, Yan Y (2009a) Biodegradation of p-nitrophenol by Rhodococcus sp. CN6 with high cell surface hydrophobicity. J Hazard Mater 163(2-3):723–728. https://doi.org/10.1016/j.jhazmat.2008.07.018
Zhang JJ, Liu H, Xiao Y, Zhang XE, Zhou NY (2009b) Identification and characterization of catabolic para-nitrophenol 4-monooxygenase and para-benzoquinone reductase from Pseudomonas sp. strain WBC-3. J Bacteriol 191(18):2703–2710. https://doi.org/10.1128/JB.01566-08
Zhang S, Sun W, Xu L, Zheng X, Chu X, Tian J, Wu N, Fan, Y (2012) Identification of the para-nitrophenol catabolic pathway, and characterization of three enzymes involved in the hydroquinone pathway, in Pseudomonas sp. 1-7. BMC Microbiol 12(1):1–11. https://doi.org/10.1186/1471-2180-12-27
Zhang X, Yang YS, Lu Y, Wen YJ, Li PP, Zhang G (2018) Bioaugmented soil aquifer treatment for P-nitrophenol removal in wastewater unique for cold regions. Water Res 144:616–627. https://doi.org/10.1016/j.watres.2018.08.004
Zheng Y, Liu D, Liu S, Xu S, Yuan Y, Xiong L (2009) Kinetics and mechanisms of p-nitrophenol biodegradation by Pseudomonas aeruginosa HS-D38. J Environ Sci 21(9):1194–1199. https://doi.org/10.1016/S1001-0742(08)62403-1
Zhongli C, Shunpeng L, Guoping F (2001) Isolation of methyl parathion-degrading strain M6 and cloning of the methyl parathion hydrolase gene. Appl Environ Microbiol 67(10):4922–4925
Zomot E, Yardeni EH, Vargiu AV, Tam HK, Malloci G, Ramaswamy VK, Perach M, Ruggerone P, Pos KM, Bibi E (2018) A new critical conformational determinant of multidrug efflux by an MFS transporter. J Mol Biol 430(9):1368–1385. https://doi.org/10.1016/j.jmb.2018.02.026
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Ma. Laura Ortiz-Hernández, Alexis Rodríguez, and Patricia Mussali-Galante conceived and designed the experiments; contributed with reagents, materials, and analysis tools; and conducted data analysis and the manuscript writing. Yitzel Gama-Martínez, Maikel Fernández-López, and Emmanuel Salazar conducted experiments. María Luisa Castrejón-Godínez prepared the figures and tables and redacted the manuscript. Sergio Encarnación and Efraín Tovar-Sánchez analyzed the data and contributed with reagents, materials, and analysis tools. All authors read and approved the manuscript.
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Ortiz-Hernández, M.L., Gama-Martínez, Y., Fernández-López, M. et al. Transcriptomic analysis of Burkholderia cenocepacia CEIB S5-2 during methyl parathion degradation. Environ Sci Pollut Res 28, 42414–42431 (2021). https://doi.org/10.1007/s11356-021-13647-6
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DOI: https://doi.org/10.1007/s11356-021-13647-6