Comparative analysis of DNA-SIP and magnetic-nanoparticle mediated isolation (MMI) on unraveling dimethoate degraders

Highlights

● Dimethoate degraders were identified via MMI and DNA-SIP.

● MMI identified Pseudomonas, Bacillus, Ramlibacter, Arthrobacter , and Rhodococcus.

● DNA-SIP identified Ramlibacter , Rhodococcus and Arthrobacter.

● Both oph B and oph C2 were involved in dimethoate metabolism.

● MMI shows higher resolution than DNA-SIP in identifying functional microbes.

Abstract

Microorganisms are crucial in the bioremediation of organophosphorus pesticides. However, most functional microorganisms (> 99%) are yet to be cultivated. This study applied two cultivation-independent approaches, DNA-SIP and magnetic-nanoparticle mediated isolation (MMI), to identify the functional microorganisms in degrading dimethoate in agricultural soils. MMI identified five dimethoate degraders: Pseudomonas, Bacillus, Ramlibacter, Arthrobacter, and Rhodococcus, whereas DNA-SIP identified three dimethoate degraders: Ramlibacter, Arthrobacter, and Rhodococcus. Also, MMI showed higher resolution than DNA-SIP in identifying functional microorganisms. Two organic phosphohydrolase (OPH) genes: ophC2 and ophB, were involved in dimethoate metabolism, as revealed by DNA-SIP and MMI. The degradation products of dimethoate include omethoate, O,O,S-trimethyl thiophosphorothioate, N-methyl-2-sulfanylacetamide, O,O-diethyl S-hydrogen phosphorodithioate, O,O,O-trimethyl thiophosphate, O,O,S-trimethyl thiophosphorodithioate, and O,O,O-trimethyl phosphoric. This study emphasizes the feasibility of using SIP and MMI to explore the functional dimethoate degraders, expanding our knowledge of microbial resources with cultivation-independent approaches.

Graphical abstract

Keywords

Stable isotope probing (SIP) / Magnetic-nanoparticle mediated isolation (MMI) / Dimethoate / Biodegradation / Cultivation-independent approach

References

[1] Ambreen S, Yasmin A, Aziz S. (2020). Isolation and characterization of organophosphorus phosphatases from Bacillus thuringiensis MB497 capable of degrading Chlorpyrifos Triazophos and Dimethoate. Heliyon, 6(7): e04221

[2] Aswathi A, Pandey A, Madhavan A, Sukumaran R K. (2021). Chlorpyrifos induced proteome remodelling of Pseudomonas nitroreducens AR-3 potentially aid efficient degradation of the pesticide. Environmental Technology & Innovation, 21: 101307

[3] Bigley A N, Raushel F M. (2013). Catalytic mechanisms for phosphotriesterases. Biochimica et Biophysica Acta. Proteins and Proteomics, 1834(1): 443–453

[4] Bouchard M F, Chevrier J, Harley K G, Kogut K, Vedar M, Calderon N, Trujillo C, Johnson C, Bradman A, Barr D B. . (2011). Prenatal exposure to organophosphate pesticides and IQ in 7-year-old children. Environmental Health Perspectives, 119(8): 1189–1195

[5] BurattiF, Testai E (2007). Evidences for CYP₃A₄ autoactivation in the desulfuration of dimethoate by the human liver. Toxicology, 241(1–2): 33–46

[6] Chen K, Liu Z, Wang X, Yu C, Ye J, Yu C, Wang F, Shen C. (2021). Enhancement of perchloroethene dechlorination by a mixed dechlorinating culture via magnetic nanoparticle-mediated isolation method. Science of the Total Environment, 786: 147421

[7] Cupples A M, Sims G K. (2007). Identification of in situ 2,4-dichlorophenoxyacetic acid-degrading soil microorganisms using DNA-stable isotope probing. Soil Biology & Biochemistry, 39(1): 232–238

[8] DebMandal M, Mandal S, Pal N K, Aich A. (2008). Potential metabolites of dimethoate produced by bacterial degradation. World Journal of Microbiology & Biotechnology, 24(1): 69–72

[9] Dumont M G, Murrell J C. (2005). Stable isotope probing-linking microbial identity to function. Nature Reviews. Microbiology, 3(6): 499–504

[10] Feng L, Jiang X, Huang Y, Wen D, Fu T, Fu R. (2021). Petroleum hydrocarbon-contaminated soil bioremediation assisted by isolated bacterial consortium and sophorolipid. Environmental Pollution, 273: 116476

[11] Feng Y C, Racke K D, Bollag J M. (1997). Isolation and characterization of a chlorinated-pyridinol-degrading bacterium. Applied and Environmental Microbiology, 63(10): 4096–4098

[12] Ishag A, Abdelbagi A O, Hammad A, Elsheikh E, Elsaid O E, Hur J H, Laing M. (2016). Biodegradation of chlorpyrifos malathion & dimethoate by three strains of bacteria isolated from pesticides polluted soils in the Sudan. Journal of Agricultural and Food Chemistry, 64(45): 8491–8498

[13] JiangBChen YXingYLianLShenY ZhangBZhang HSunGLiJWangX ZhangD (202202). Negative correlations between cultivable and active-yet-uncultivable pyrene degraders explain the postponed bioaugmentation. Journal of Hazardous Materials, 423423: 127189

[14] Jiang B, Jin N, Xing Y, Su Y, Zhang D. (2018). Unraveling uncultivable pesticide degraders via stable isotope probing (SIP). Critical Reviews in Biotechnology, 38(7): 1025–1048

[15] Jiang L, Song M, Luo C, Zhang D, Zhang G. (2015). Novel phenanthrene-degrading bacteria identified by DNA-stable isotope probing. PLoS One, 10(6): e0130846

[16] Li J, Luo C, Song M, Dai Q, Jiang L, Zhang D, Zhang G. (2017a). Biodegradation of phenanthrene in polycyclic aromatic hydrocarbon-contaminated wastewater revealed by coupling cultivation-dependent and -independent approaches. Environmental Science & Technology, 51(6): 3391–3401

[17] Li J, Luo C, Zhang G, Zhang D. (2018). Coupling magnetic-nanoparticle mediated isolation (MMI) and stable isotope probing (SIP) for identifying and isolating the active microbes involved in phenanthrene degradation in wastewater with higher resolution and accuracy. Water Research, 144: 226–234

[18] Li J, Zhang D, Song M, Jiang L, Wang Y, Luo C, Zhang G. (2017b). Novel bacteria capable of degrading phenanthrene in activated sludge revealed by stable-isotope probing coupled with high-throughput sequencing. Biodegradation, 28(5–6): 423–436

[19] Li R, Zheng J, Wang R, Song Y, Chen Q, Yang X, Li S, Jiang J. (2010). Biochemical degradation pathway of dimethoate by Paracoccus sp. Lgjj-3 isolated from treatment wastewater. International Biodeterioration & Biodegradation, 64(1): 51–57

[20] Lian L, Jiang B, Xing Y, Zhang N. (2021). Identification of photodegradation product of organophosphorus pesticides and elucidation of transformation mechanism under simulated sunlight irradiation. Ecotoxicology and Environmental Safety, 224: 112655

[21] Lian L, Xing Y, Zhang N, Jiang B. (2022). Identification of chlorpyrifos-degrading microorganisms in farmland soils via cultivation-independent and -dependent approaches. Environmental Science. Processes & Impacts, 24(7): 1050–1059

[22] Liang J, Gao S, Wu Z, Rijnaarts H H M, Grotenhuis T. (2021). DNA-SIP identification of phenanthrene-degrading bacteria undergoing bioaugmentation and natural attenuation in petroleum-contaminated soil. Chemosphere, 266: 128984

[23] Liu T, Xu S, Lu S, Qin P, Bi B, Ding H, Liu Y, Guo X, Liu X. (2019). A review on removal of organophosphorus pesticides in constructed wetland: performance, mechanism and influencing factors. Science of the Total Environment, 651: 2247–2268

[24] Maggi F, Tang F, Black A J, Marks G B, Mcbratney A. (2021). The pesticide health risk index: an application to the world’s countries. Science of the Total Environment, 801: 149731

[25] Pan X, Dong F, Wu X, Xu J, Liu X, Zheng Y. (2019). Progress of the discovery, application, and control technologies of chemical pesticides in china. Journal of Integrative Agriculture, 18(4): 840–853

[26] Rolando L, Grenni P, Rauseo J, Pescatore T, Patrolecco L, Garbini G L, Visca A, Barra Caracciolo A. (2020). Isolation and characterization in a soil conditioned with foaming agents of a bacterial consortium able to degrade sodium lauryl ether sulfate. Frontiers in Microbiology, 11: 1542

[27] Sahin C, Karpuzcu M E. (2020). Mitigation of organophosphate pesticide pollution in agricultural watersheds. Science of the Total Environment, 710: 136261

[28] Shen Y, Jiang B, Xing Y. (2021). Recent advances in the application of magnetic Fe₃O₄ nanomaterials for the removal of emerging contaminants. Environmental Science and Pollution Research International, 28(7): 7599–7620

[29] Singh B, Walker A, Wright D. (2006). Bioremedial potential of fenamiphos and chlorpyrifos degrading isolates: influence of different environmental conditions. Soil Biology & Biochemistry, 38(9): 2682–2693

[30] Singh B K, Walker A. (2006). Microbial degradation of organophosphorus compounds. FEMS Microbiology Reviews, 30(3): 428–471

[31] Teng T, Liang J, Wu Z. (2021). Identification of pyrene degraders via DNA-SIP in oilfield soil during natural attenuation, bioaugmentation and biostimulation. Science of the Total Environment, 800: 149485

[32] Thomas C M, Nielsen K M. (2005). Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nature Reviews. Microbiology, 3(9): 711–721

[33] Wang B, Teng Y, Yao H, Christie P. (2021). Detection of functional microorganisms in benzene [a] pyrene-contaminated soils using DNA-SIP technology. Journal of Hazardous Materials, 407: 124788

[34] Wang X, Zhao X, Li H, Jia J, Liu Y, Ejenavi O, Ding A, Sun Y, Zhang D. (2016). Separating and characterizing functional alkane degraders from crude-oil-contaminated sites via magnetic nanoparticle-mediated isolation. Research in Microbiology, 167(9–10): 731–744

[35] Warhurst A M, Fewson C A. (1994). Biotransformations catalyzed by the genus Rhodococcus. Critical Reviews in Biotechnology, 14(1): 29–73

[36] Yu J, Bian Z, Tian X, Zhang J, Zhang R, Zheng H. (2018). Atrazine and its metabolites in surface and well waters in rural area and its human and ecotoxicological risk assessment of Henan Province, China. Human and Ecological Risk Assessment, 24(1): 1–13

[37] Zhang D, Berry J P, Zhu D, Wang Y, Chen Y, Jiang B, Huang S, Langford H, Li G, Davison P A. . (2015). Magnetic nanoparticle-mediated isolation of functional bacteria in a complex microbial community. ISME Journal, 9(3): 603–614

[38] Zhao X, Li H, Ding A, Zhou G, Sun Y, Zhang D. (2016). Preparing and characterizing Fe₃O₄@cellulose nanocomposites for effective isolation of cellulose-decomposing microorganisms. Materials Letters, 163: 154–157

[39] Zhou J, Li X, Jiang Y, Wu Y, Chen J, Hu F, Li H. (2011). Combined effects of bacterial-feeding nematodes and prometryne on the soil microbial activity. Journal of Hazardous Materials, 192(3): 1243–1249

[40] ZhuF, Zhu C, Doyle E, Liu H, Zhou D, Gao J (2018). Fate of di(2-ethylhexyl) phthalate in different soils and associated bacterial community changes. Science of the Total Environment, 637–638: 460–469

Acknowledgements

The authors would like to thank the National Natural Science Foundation of China (Nos. 42177359 and 41807119), the Natural Science Foundation of Beijing (No. 8212030), the Fundamental Research Funds for the Central Universities (Nos. FRF-TP-20-010A3 and FRF-IDRY-22-001), and the Open Fund of National Engineering Laboratory for Site Remediation Technologies (No. NEL-SRT201907).

Conflict of Interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Electronic Supplementary Material

Supplementary material is available in the online version of this article at https://doi.org/10.1007/s11783-024-1765-x and is accessible for authorized users.

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