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.
Similar content being viewed by others
References
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
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
Bigley A N, Raushel F M (2013). Catalytic mechanisms for phosphotriesterases. Biochimica et Biophysica Acta. Proteins and Proteomics, 1834(1): 443–453
Bouchard M F, Chevrier J, Harley K G, Kogut K, Vedar M, Calderon N, Trujillo C, Johnson C, Bradman A, Barr D B, et al. (2011). Prenatal exposure to organophosphate pesticides and IQ in 7-year-old children. Environmental Health Perspectives, 119(8): 1189–1195
Buratti F, Testai E (2007). Evidences for CYP3A4 autoactivation in the desulfuration of dimethoate by the human liver. Toxicology, 241(1–2): 33–46
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
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
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
Dumont M G, Murrell J C (2005). Stable isotope probing-linking microbial identity to function. Nature Reviews. Microbiology, 3(6): 499–504
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
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
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
Jiang B, Chen Y, Xing Y, Lian L, Shen Y, Zhang B, Zhang H, Sun G, Li J, Wang X, Zhang D (2022). Negative correlations between cultivable and active-yet-uncultivable pyrene degraders explain the postponed bioaugmentation. Journal of Hazardous Materials, 423 (Pt B): 127189
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
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
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
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
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
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
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
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
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
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
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
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
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
Sahin C, Karpuzcu M E (2020). Mitigation of organophosphate pesticide pollution in agricultural watersheds. Science of the Total Environment, 710: 136261
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
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
Singh B K, Walker A (2006). Microbial degradation of organophos-phorus compounds. FEMS Microbiology Reviews, 30(3): 428–471
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
Thomas C M, Nielsen K M (2005). Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nature Reviews. Microbiology, 3(9): 711–721
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
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
Warhurst A M, Fewson C A (1994). Biotransformations catalyzed by the genus Rhodococcus. Critical Reviews in Biotechnology, 14(1): 29–73
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
Zhang D, Berry J P, Zhu D, Wang Y, Chen Y, Jiang B, Huang S, Langford H, Li G, Davison P A, et al. (2015). Magnetic nanoparticle-mediated isolation of functional bacteria in a complex microbial community. ISME Journal, 9(3): 603–614
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
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
Zhu F, 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).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
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.
Additional information
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 ophB and ophC2 were involved in dimethoate metabolism.
• MMI shows higher resolution than DNA-SIP in identifying functional microbes.
Rights and permissions
About this article
Cite this article
Lian, L., Xing, Y., Zhang, D. et al. Comparative analysis of DNA-SIP and magnetic-nanoparticle mediated isolation (MMI) on unraveling dimethoate degraders. Front. Environ. Sci. Eng. 18, 5 (2024). https://doi.org/10.1007/s11783-024-1765-x
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11783-024-1765-x