doi: 10.1007/s12571-015-0446-9, Ayalew, T (2014). On the other hand, isolate T2, despite being able to remove the fungicides at some extent, in most cases was unable to detoxify the matrix, making this fungus an unsuitable choice for biodegradation. These combined results show that MMV668754/Trifloxystrobin is effective in killing infected bovine leukocytes and is comparable with Buparvaquone treatment in targeting T. annulata and T. parva schizonts in bovine lymphocytes and macrophages. Isolates were grown in Petri plates with potato-dextrose-agar (PDA) (DifcoTM Laboratories, Detroit, Michigan, U.S.A.) for ca. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher. The colony growth of infected TBL3 cells was completely blocked by Buparvaquone and significantly reduced by adding MMV668754 [Fig. Sci. M.V., N.L., J.B. and S.L. Woods, K. L. et al. Evolution of habitat preference and nutrition mode in a cosmopolitan fungal genus with evidence of interkingdom host jumps and major shifts in ecology. Chemosphere 112, 526530. a TaC12 infected macrophages were incubated at 37C or at 41C for 810days to induce merogony. An acute toxicity test was performed with the freshwater microcrustacean D. magna using untreated samples (initial work pesticide solutions in liquid culture media) and samples collected after 14 days for each treatment (abiotic and heat-killed controls, and viable fungus). For cell cycle analysis, cells at 1104/ml were stained with propidium iodide (PI) after different drug treatments. We gratefully acknowledge the Medicines for Malaria Venture (MMV, Geneva, Switzerland) for providing the MMV Pathogen Box compound library. Cock-Rada, A. M. et al. Chemosphere 186, 625634. Trifloxystrobin Metabolite CGA 321113 is . 8, 134 (2020). Article Results are shown for T. annulata-infected macrophages (TaC12), B lymphocytes (TBL3) or T. parva-infected (TpM) lymphocytes. Food Chem. from the endosphere of wild Rubiaceae was performed to test their fungicide biodegradation potential. Rikxoort, H., Schroth, G., Lderach, P., and Rodrguez-Snchez, B. Chemosphere 144, 864871. The grid points in X, Y and Z axis were set at 757575 with a grid-spacing of 0.303. Leveraging the medicines for Malaria Venture malaria and pathogen boxes to discover chemical inhibitors of East Coast fever. Mixtures were diluted 1000-fold, and TaPin1 activity was assayed for 1min by reading the absorbance at 380nm. As MMV668754/Trifloxystrobin treatment did not cause extensive apoptosis in TaC12 macrophages we also tested the effect on the ability of surviving Theileria parasites to differentiate to merozoites [Fig. Biodegradation of chlorothalonil in soil after suppression of degradation. Other mycoparasitic Trichoderma species, e.g., T. inhamatum, besides its reported use as a biocontrol agent, is also capable of transforming a highly toxic chromium into a less harmful form (Morales-Barrera and Cristiani-Urbina, 2008). Van Voorhis, W. C. et al. Moreover, its mycoparasitism mechanism remained even in the presence of azoxystrobin (da Silva et al., 2018). 1a]. Agroecol. doi: 10.1371/journal.pone.0146021, Robbertse, B., Strope, P., Chaverri, P., Gazis, R., and Schoch, C. L. (2017). a Chemical structures of DTM (Pin1 inhibitor) and the test compound MMV688754. Mean valuesSD. Trichoderma resistance to trifloxystrobin has been previously reported (Kosanovi et al., 2015); however, according to our results, efficiency ascribed to biodegradation was quite low for this fungicide. Biotransformation 29, 119129. Nugraha, A. We previously demonstrated that microscopy-based screens followed by careful phenotypic characterization present a powerful drug-discovery strategy24. doi: 10.1016/j.biocontrol.2008.01.003, Bayramoglu, G., and Arica, M. Y. (2021). Progress towards understanding the immunobiology of Theileria parasites. We expect that compounds which kill the parasite would also result in host cell apoptosis and reduced host cell survival25. . PLoS Pathog. 1a]. Proteins were stored at 80C until used. Nyagwange, J. et al. PLoS ONE 6:e024528. Isolate T4 also exhibited an intermediate efficiency, while isolate T2 was unable to detoxify the matrix in most cases. Assess. J. Environ. B. Intracellular Theileria parasites PIN down host metabolism. Fungal Biol. Resulting plasmids were sequenced (Eurofins) and sequences were manually checked to correct possible base calling errors. The bacteria were pelleted by centrifugation (2000 g, 20min), washed with cold PBS, and harvested by centrifugation (2000 g, 15min). Modelling the impact of climate change on the interaction between grapevine and its pests and pathogens: European grapevine moth and powdery mildew. We defined a threshold for the Schizont/Merogony cycle stage of 50 parasites per host cell. Therefore, fungi that act as biocontrollers may also be capable of degrading residual pesticides in the fields or within plants, representing an important tool, not only for the transition from conventional to organic agriculture, but to complement different disease management strategies and recovery of healthy soil microbiomes. Rev. Biodegradation of pentachlorophenol by marine-derived fungus Trichoderma harzianum CBMAI 1677 isolated from ascidian Didemnun ligulum. Open source drug discovery with the Malaria box compound collection for neglected diseases and beyond. (2021). (2021). Trifloxystrobin acid (TFSA) (Fig. For example, T1, which was able to grow in presence of all fungicides, produced mycelium, but not conidia in some cases. Except for T2 (EC50 = 0.088%), whose toxicity was lower than the abiotic control, but slightly higher than that of the respective HKC, further detoxification was obtained in Rxn treatments T1 (EC50 = 7.4%) and T4 (EC50 = 5.1%). Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. PubMed The combination of pesticide tolerance, removal, and ecotoxicity assays with biocontrol or bioremediation microorganisms, and interactions between agrochemicals, should be considered in the development of sustainable agriculture strategies. 3a], but only two compounds (MMV688372 and MMV668754) demonstrated selective killing of infected TBL3 cells compared to uninfected cells (>80% survival) [Fig. Host cells (at least n=50) were assessed for each experiment and parasite nuclei (DAPI staining) per host cell were counted manually. Int. This work was supported by the French National Research Agency (ANR PATHO-METHYLOME #ANR-15-CE12-0020), the EUR G.E.N.E. doi: 10.1007/BF00335964, Murillo-Zamora, S., Castro-Gutirrez, V., Mass-Mora, M., Lizano-Fallas, V., and Rodrguez-Rodrguez, C. E. (2017). Agric. These experiments were done in the dark to avoid degradation by photolysis. J. Cell. Biol. We developed a microscopy-based screen to reposition drugs from the open-access Medicines for Malaria Venture (MMV) Pathogen Box. In cyproconazole, toxicity in the abiotic control decreased after 14 d (EC50 = 3.6%) with respect to the initial solution (EC50 = 1.09%). 4, 266275. Toxicol. n=3 independent experiments. Coffee in the crosshairs of climate change: agroforestry as abatis. Nusant. 5b]. (2018). The concentrations of the active ingredients according to the commercial label are listed in Supplementary Table 2. Maximum To measure cell viability, 1104 cells were plated in 96-well plates in triplicate before MMV drug treatments for 48h. Cell viability was measured using the Cell Proliferation Kit IIXTT (Roche) and the GloMax-Multi Detection System (Promega) following manufacturers instructions. Meanwhile, propineb (P = 0.704234), validamycin-A (P = 0.7296269), and trifloxystrobin (P = 0.3721598) had similar effect over the fungi. Freund's adjuvants, and o-phenylenediamine were purchased from Sigma/Aldrich (Madrid, Spain). We chose to study the MMV668754/Trifloxystrobin compound in further detail. Trifloxystrobin Metabolite CGA 321113 Synonym(s) : ( E )--Methoxyimino-2-[( E )-1-(3-trifluoromethylphenyl)ethylidenaminooxymethyl]phenylacetic acid, Trifloxystrobin acid Empirical Formula (Hill Notation) : C 19 H 17 F 3 N 2 O 4 Sci. Cells were cultured in RPMI 1640 (Gibco-BRL), supplemented with 10% heat-inactivated fetal bovine serum (FBS), 4 mM L-glutamine, 25mM HEPES, 10mM -mercaptoethanol and 100mg/ml of penicillin/streptomycin in a humidified 5% CO2 atmosphere at 37C. Trifloxystrobin has low acute oral, dermal and inhalation toxicity. doi: 10.1007/s13593-014-0223-8, Ritz, C., Baty, F., Streibig, J. C., and Gerhard, D. (2015). Food Addit. Therefore, sustainable and environmentally friendly disease management strategies, such as biological control, are urgently needed (Ayalew, 2014; Rice, 2018). The Buparvaquone drug is shown in brown and the two compounds MMV688372 and MMV688754 used in subsequent experiments are colored orange. Chapter 37 - Herbicides and Fungicides, in Reproductive and Developmental Toxicology, ed. Chemosphere 221, 403411. Cytochrome B has also been described as a MMV668754/Trifloxystrobin target in other microorganisms36. Both compounds are effective against both T. annulata and T. parva species, as well as different host cell types (macrophages or lymphocytes). Our microscopy screening approach recorded a number of parameters including host nuclei number, parasite schizont structure and the parasite load per host cell. The merogony differentiation process can be induced by incubating infected macrophages at 41C for 8days. Int. However, in the case of azoxystrobin, high removal occurred by adsorption (Figure 3A1). 162, 19. National University of Ro Cuarto, Argentina, Escuela de Ciencias y Tecnologas, Universidad de Concepcion, Chile. To determine whether the fungal removal process is environmentally relevant, an ecotoxicological assay was employed to confirm detoxification, as some transformation products from pesticide degradation might present higher toxicity than the original compound (Ruz-Hidalgo et al., 2016). doi: 10.1016/j.ibiod.2017.07.008, Clinton, B., Warden, A. C., Haboury, S., Easton, C. J., Kotsonis, S., Taylor, M. C., et al. 191, 128132 (2019). 8b]. Mutations in the TaPIN1 peptidyl prolyl isomerase gene in Theileria annulata parasites isolated in Sudan. Default protocol was applied, with an initial population of 150 randomly placed individuals, a maximum number of 2.5105 energy evaluations, and a maximum number of 2.7104 generations. (2019). (2014). doi: 10.1038/s41598-017-07807-3, Cheng, Z., Li, C., Kennes, C., Ye, J., Chen, D., Zhang, S., et al. b Purification of recombinant His-tagged TaPin1 protein. Adsorption to the fungal biomass was only observed at a low extent for T2 (5.3%) (Figure 3C1,C2). Food Chem. Images were generated and processed using Metamorph and ImageJ software. Plant Dis. Perspect. All data generated or analysed during this study are included in this published article (and its supplementary information files). Nonetheless, in one study, biodegradation of four triazoles with T. versicolor could not be achieved, even after fungal re-inoculation (Murillo-Zamora et al., 2017). An alternative and rich guild of microorganisms adapted to these conditions are endophytic fungi, which inhabit the interior tissue of plants without causing apparent disease symptoms, facilitate plant adaptation to the environment, and may act as antagonists against phytopathogens; thus, they can be used as biological control and bioremediation agents (Harman, 2007; Howell, 2007; Stamatiu-Snchez et al., 2014; Deng and Cao, 2017; Khan and Mohiddin, 2018; Holanda et al., 2019; Pietro-Souza et al., 2020). Environ. Wood Fiber Sci. Figure 1. These include the induction of signaling pathways (such as JNK/AP-1 or Myc), the sequestration of host proteins (such as IKK or EB1) and the secretion of effectors11,13,14,15,16,17,18,19. Clim. Google Scholar. 41, 157167. Rachel H. Clare, Catherine Bardelle, Stephen A. The images or other third party material in this article are included in the articles Creative Commons license, unless indicated otherwise in a credit line to the material. The role of sorption processes in the removal of pharmaceuticals by fungal treatment of wastewater. In addition, healthy soil microbiomes and ecosystems could be enhanced if biocontrol microorganisms aided in bioremoval or biodegradation of accumulated fungicides (Komrek et al., 2010; Roman et al., 2021). Food Contam. The most effective of these, by far, was the MMV668754 compound which corresponds to the drug Trifloxystrobin. No growth inhibition was observed for strobilurins. AC, Abiotic control; HKC, Heat-killed control; Rxn, viable fungal biomass treatment. (2021). 38, 17051715 (2008). Biodegrad. T. annulata-infected macrophages (TaC12 cell line) were distributed into 96-well plates and imaged after incubation (48h) with compounds from the MMV Pathogen Box library at two concentrations. We chose to use the T. annulata-infected bovine macrophage cell line TaC12, because of ease of imaging and parasite monitoring. In the meantime, to ensure continued support, we are displaying the site without styles doi: 10.1021/jf00011a027, Schoch, C. L., Seifert, K. A., Huhndorf, S., Robert, V, Spouge, J. L., Levesque, A., et al. Trifloxystrobin Metabolite CGA 321113 PESTANAL, analytical standard; CAS Number: 252913-85-2; Synonyms: (E)--Methoxyimino-2-[(E)-1-(3-trifluoromethylphenyl)ethylidenaminooxymethyl]phenylacetic acid,Trifloxystrobin acid; find Supelco-34518 MSDS, related peer-reviewed papers, technical documents, similar products & more at Sigma-Aldrich Biodegradation mechanism of 1H-1,2,4-Triazole by a newly isolated strain Shinella sp. Even though the four isolates were able to tolerate and grow with most fungicides, some changes in the morphology patterns were observed after 15 days (Figure 2). Acad. n=3 independent experiments. Interestingly, at least one of these (V227M) was previously reported in field samples of Buparvaquone resistance9. Biol. Our study involved a series of increasingly stringent assays to select the more promising drug compound from the MMV Pathogen Box library4. Rep. 2017, 137. Cancer Res. Available online at: https://www.R-project.org/, Ramrez-Morales, D., Mass-Mora, M., Beita-Sand, W., Montiel-Mora, J. R., Fernndez-Fernndez, E., Mndez-Rivera, M., et al. ****p<0.0001. One of the most affected regions is Central America, where coffee farmers are mainly small and low-income (Davis et al., 2012; Paterson et al., 2014; Rikxoort et al., 2014; Avelino et al., 2015; Talhinhas et al., 2017; Verhage et al., 2017). Phytopathology 109, 18881899. Z., Guo, R. J., Takagi, K., Miao, Z. Q., and Li, S. D. (2011). Conjugation of 2-chloroacetanilide herbicides with glutathione: role of molecular structures and of glutathione s-transferase enzymes. Isolation and characterisation of azoxystrobin degrading bacteria from soil. The different responses of glutathione-dependent detoxification pathway to fungicide chlorothalonil and carbendazim in tomato leaves. Schmuckli-Maurer, J., Shiels, B. Theileria highjacks JNK2 into a complex with the macroschizont GPI (GlycosylPhosphatidylInositol)-anchored surface protein p104. Ultra-pure deionised water was purified by Millipore ultra-pure system to a specific resistance of 18 m cm (Synergy Water Purification System, Millipore). Neurotoxicity assessment of QoI strobilurin fungicides azoxystrobin and trifloxystrobin in human SH-SY5Y neuroblastoma cells: Insights from lipidomics and mitochondrial bioenergetics. A remarkable feature of Theileria spp is the ability to induce transformation of host leukocytes11,13. (#ANR-17-EURE-0013), and the Who Am I? Laboratory of Excellence #ANR-11-LABX-0071 funded by the French Government through its Investments for the Future program operated by the ANR under grant #ANR-11-IDEX-0005-01, the Fondation ARC pour la Recherche sur le Cancer (ARC n228308_ARCP, AAP ARC 2020 PJA3), the PARA-SET project funded by IDEX UP AAP EMERGENCE (#IDEX-2021-I-053). In May 2023, Frontiers adopted a new reporting platform to be Counter 5 compliant, in line with industry standards. (2019). & Hemphill, A. 72, 810820 (2012). 8a]. One advantage of our screening strategy is the additional information gleaned from the microscopic data. Int. ns=not significant, ****p<0.001. The supernatant was incubated 2h on ice in the presence of 10mM imidazole and His-select nickel beads (Sigma). Biodegradation 154:105049. doi: 10.1016/j.ibiod.2020.105049, Jaramillo, J., Muchugu, E., Vega, F. E., Davis, A., Borgemeister, C., and Chabi-Olaye, A. Mhadhbi, M., Chaouch, M., Ajroud, K., Darghouth, M. A. 187, 431435 (2012). (2018). Table 1. Total fungicide removal ranged from 26.8 to 33.1% for all tested strains. Two-way Anova statistical test, Dunnetts multiple comparison: *p<0.05, **p<0.01, ***p<0.001, ****p<0.0001. Taxonomic accuracy for fungi in public sequence databases: applying One name one species' in well-defined genera with Trichoderma/Hypocrea as a test case. Front. The Meeting estimated a maximum residue level of 0.05* mg/kg and an STMR of 0 for trifloxystrobin in asparagus. In general, information regarding strobilurins biodegradation is limited. We developed a microscopy-based strategy for screening the MMV Pathogen Box library of compounds that allowed for high-content assessment of the drug impact. Chemosphere 272:129574. doi: 10.1016/j.chemosphere.2021.129574, Ramirez-Villegas, J., Salazar, M., Jarvis, A., and Navarro-Racines, C. E. (2012). It is known that species within the T. harzianum complex have the capacity to metabolize and tolerate tebuconazole, another triazole (Obanda and Shupe, 2009). Results are plotted for percent host cell survival, with the darkest spots representing compounds causing <25% survival. doi: 10.1371/journal.pone.0047981, Deng, Z., and Cao, L. (2017). International biodeterioration & biodegradation degradation of chlorothalonil via thiolation and nitrile hydration by marine strains isolated from the surface seawater of the Northwestern Pacific. Sci. doi: 10.1021/jf3025634, Stamatiu-Snchez, K., Alarcn, A., Ferrera-Cerrato, R., Nava-Daz, C., Snchez-Escudero, J., Cruz-Snchez, J. S., et al. Biol. Our study suggests that Trifloxystrobin could provide an effective alternative to Buparvaquone treatment and represents a promising candidate for future drug development against Theileria spp. Article Cell Dev. In addition, T. harzianum has been reported to achieve complete biotransformation of pentachlorophenol (Vacondio et al., 2015), a halogenated substituted monocyclic aromatic fungicide which exhibits a strong similarity to chlorothalonil at the chemical structure level (Gupta, 2017). Res. volume5, Articlenumber:1253 (2022) In (A1D1), numbers in Y axis (g/L) refer to concentration of active ingredient. The MMV668754 compound was as effective as the care-standard Buparvaquone drug in nearly all the assays we tested. Representative of three independent experiments. Commercial fungicides were added to the PDB media according to the recommended dose for coffee (Supplementary Table 2). Trifloxystrobin treatment reduced parasite load in vitro as effectively as Buparvaquone, with similar effects on host gene expression, cell proliferation and cell cycle. Continuous treatment of clofibric acid by Trametes versicolor in a fluidized bed bioreactor: Identification of transformation products and toxicity assessment. Rational design of highly potent and slow-binding cytochrome bc1 inhibitor as fungicide by computational substitution optimization. Protein expression was then induced by adding 500M isopropyl-1-thio--D-galactopyranosid (IPTG) and lowering the temperature to 16C overnight. Hemphill and colleagues recently proposed an elegant quantitative RT-PCR assay for assessing drug activities against intracellular Theileria schizonts30. Docked conformations were then clustered using a RMSD threshold of 1.0 . We compared these hit compounds with those from previously reported screens of the MMV library against T. annulata, T. parva or T. equi parasites [Fig. 42, 215226 (2020). Sci. Trifloxystrobin Synonyms: Methyl (E)--methoxyimino-2- [ (E)-1- (3-trifluoromethylphenyl)ethylidenaminooxymethyl]phenylacetate Empirical Formula (Hill Notation): C20H19F3N2O4 CAS Number: 141517-21-7 Molecular Weight: 408.37 Product Comparison Guide Use the product attributes below to configure the comparison table. Despite the similarity in the effects of MMV668754 and Buparvaquone in all the functional assays, we show that their modes of action are likely to be distinct; MMV668754 did not inhibit the catalytic activity of the TaPin1 prolyl isomerase which was reported to be mutated in some Buparvaquone-resistant parasites6,7. In previous studies, chlorothalonil biodegradation was reported by some bacteria such as Sphingobium spp., Stenotrophomonas spp., and Ochrobactrum lupini, among others (Motonaga et al., 1996; Van Eeden et al., 2000; Shi et al., 2011; Man-yun et al., 2014; Hu et al., 2020). EE-L, PA-V, and CR-R analyzed the data. doi: 10.1016/j.foodres.2014.03.037, Pietro-Souza, W., de Campos Pereira, F., Mello, I. S., Stachack, F. F. F., Terezo, A. J., Cunha, C. N., et al. Change 115, 611628. to grow in the presence of fungicides in solid phase; and (ii) evaluate their capacity to remove and detoxify different fungicides in liquid medium through analytical and ecotoxicological tests. Publishers note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. The fungicides were added to the PDA after media sterilization to avoid their degradation. The result obtained with cyproconazole (Figure 1A) was particularly noteworthy because after 5 days of evaluation it produced the highest inhibition on Trichoderma isolates T2, T3, and T4, being T1 the only one able to grow (37 mm) in the presence of this compound. Isolate T4 also exhibited an intermediate efficiency, although with lower detoxification capacity than T1. Polymerase Chain Reactions (PCR) were prepared using primers ITS 4 and ITS 5 (Schoch et al., 2012) for internal transcribed spacers nuclear ribosomal DNA (ITS); EF728Mf and EF1R primers (Carbone and Kohn, 1999) for a partial region of translation elongation factor 1-alpha (TEF); and RPB25F and RPB2-7CR primers (Liu et al., 1999) for a partial region of RNA polymerase II subunit (RPB2). stand apart from other apicomplexa parasites by their ability to transform host leukocytes into immortalized, hyperproliferating, invasive cells that rapidly kill infected animals. Consumer motives for purchasing organic coffee: The moderating effects of ethical concern and price sensitivity. Crop Prot. (2016). AutoDock4 and AutoDockTools4: automated docking with selective receptor flexibility. performed the structural modeling analysis. Chemosphere 198, 198203. All test substances (azoxystrobin, terbutryn, prochloraz, diclofenac, trifloxystrobin) were purchased from Sigma-Aldrich. 4b]. However, its adverse effects on aquatic organisms remain unknown. B. Parasitol. Further information on research design is available in theNature Research Reporting Summary linked to this article. c Cell cycle analysis by flow cytometry performed on BL3 and TBL3 cells following treatment with 2M drugs for 48h. Error bars represent mean valuesSD. The results from this study will contribute to the design of disease management strategies that include biocontrol agents that tolerate chemical fungicides and can, at the same time, colonize soil and the plant endosphere. Slider with three articles shown per slide. Final biodegradation was 8.5% for T2 and 12.7% for T4. Briefly, sets of 10 daphnid neonates (<24 h) were placed in 25 mL vials and exposed to 10 mL of each dilution of the sample (prepared in moderately hard reconstituted water); triplicate sets per dilution were incubated in the dark at 23 1C for 48 h. After incubation, immobility was determined and assumed as mortality. Cells were washed in PBS, fixed in ice-cold ethanol (70% v/v) and stored at 4C. (2010). Int. This compound was more effective at reducing host cell survival and parasite cell number than Buparvaquone, the standard-of-care drug to treat Theileria-infected cows [Fig. In the case of azoxystrobin, the highest removal (82.2%) occurred by adsorption to fungal biomass. Kruskal Wallis non-parametric test followed by Dunns multiple comparison test. ns=not significant, ****p<0.0001. b Quantification of the percentage of cells at the macroschizont or merogony stage after 810days in culture at 41C, with or without MMV688754, or DMSO treatments.
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