Evaluation of the Impact of Flutriafol on Soil Culturable Microorganisms and on Soil Enzymes Activity
Abstract
:1. Introduction
2. Materials and Methods
2.1. Fungicide
2.2. Soil Sampling
2.3. Assessment of the Effects of Flutriafol on Populations of Soil Culturable Microorganisms
2.4. Evaluation of the Effects of Flutriafol on Soil Enzyme Activities
2.5. Molecular Docking Study
Enzyme | Microorganism | Description and PDB/AlphaFold ID |
---|---|---|
Dehydrogenase | Clostridium beijerinckii | NADP-dependent alcohol dehydrogenase in complex with dihydro-nicotinamide-adenine-dinucleotide phosphate and Zn ion (1KEV chain A) [28] |
Aspergillus fumigatus | Mannitol 2-dehydrogenase in complex with 1,4-dihydronicotinamide adenine dinucleotide (7RK5 chain A) [29] | |
Rhizobium leguminosarum | Succinate semialdehyde dehydrogenase in complex with 1,4-dihydronicotinamide adenine dinucleotide (8C54 chain A) [30] | |
Urease | Bacillus pasteurii | Urease subunit gamma in complex with citrate anion, 1,2-ethanediol, hydroxide, nickel (II), and sulfate ions (4AC7 chain C) [31] |
Aspergillus fumigatus | AlphaFold model of catalase AF-Q6A3P9-F1 [27] | |
Rhizobium leguminosarum | AlphaFold model of catalase AF-Q1MCV9-F1 [27] | |
Phosphatase | Bacillus subtilis | Phosphate phosphatase F in complex with its inhibitory peptide GLN-ARG-GLY-MET-ILE (4I9C chain A) [32] |
Aspergillus niger | Acid phosphatase in complex with oligosaccharides, 2-acetamido-2-deoxy-beta-D-glucopyranose, glycerol, and sulfate ion (1QFX chain A) [33] | |
Rhizobium leguminosarum | Alkaline phosphatase in complex with acetate, manganese (II), calcium, and sodium ions (2VQR chain A) [34] | |
Catalase | Micrococcus lysodeikticus | Catalase complexed with dihydro-nicotinamide-adenine-dinucleotide phosphate and hem (1GWH chain A) [35] |
Komagataella pastoris | Catalase in complex with hem, dihydro-nicotinamide-adenine-dinucleotide phosphate, di(hydroxyethyl)ether, glycerol, sulfate, sodium, chloride and potassium ions (6RJN chain A) [36] | |
Rhizobium meliloti | AlphaFold model of catalase AF-Q9X576-F1 [27] |
2.6. Statistical Analysis
3. Results
3.1. Assessment of the Effects of Flutriafol on Soil Microbiota
3.2. Assessment of the Effects of Flutriafol on Activities of Soil Enzymes
3.3. Molecular Docking Analysis of the Interactions between the Flutriafol Enantiomers and Investigated Soil Enzymes
4. Discussion
4.1. Evaluation of the Effects of Flutriafol on Populations of Soil Culturable Microorganisms
4.2. Evaluation of the Effects of Flutriafol on Soil Enzyme Activities
4.3. Molecular Docking Analysis
4.4. Factors Affecting the Impact of Pesticides on Soil and Crops and Remediation Solutions
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Data Availability Statement
Conflicts of Interest
References
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Dose/ Time (Days) | p Values | ||||||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Control | 1/2D | D | 2D | ||||||||||||||
7 | 14 | 21 | 28 | 7 | 14 | 21 | 28 | 7 | 14 | 21 | 28 | 7 | 14 | 21 | 28 | ||
Control | 7 | 0.98 | 0.01 | 0.14 | 0.91 | 0.20 | 0.06 | 0.01 | 0.94 | 0.04 | 0.02 | <0.05 | 0.78 | 0.04 | 0.01 | <0.01 | |
14 | 1.00 | 0.01 | 0.13 | 0.88 | 0.19 | 0.06 | 0.01 | 0.97 | 0.04 | 0.02 | 0.04 | 0.76 | 0.04 | 0.01 | <0.01 | ||
21 | 0.96 | 0.99 | 0.30 | 0.02 | 0.22 | 0.52 | 0.98 | 0.01 | 0.65 | 0.85 | 0.60 | 0.03 | 0.63 | 0.87 | 0.56 | ||
28 | 0.02 | 0.04 | 0.49 | 0.18 | 0.84 | 0.69 | 0.31 | 0.12 | 0.56 | 0.40 | 0.61 | 0.23 | 0.58 | 0.23 | 0.11 | ||
1/2D | 7 | 1.00 | 1.00 | 0.97 | 0.02 | 0.25 | 0.08 | 0.02 | 0.85 | 0.05 | 0.03 | 0.06 | 0.87 | 0.06 | 0.01 | <0.01 | |
14 | 1.00 | 1.00 | 0.68 | <0.01 | 1.00 | 0.55 | 0.23 | 0.18 | 0.43 | 0.29 | 0.47 | 0.32 | 0.45 | 0.16 | 0.07 | ||
21 | 1.00 | 1.00 | 1.00 | 0.28 | 1.00 | 0.88 | 0.54 | 0.05 | 0.85 | 0.65 | 0.91 | 0.11 | 0.87 | 0.42 | 0.22 | ||
28 | <0.01 | <0.01 | 0.07 | 1.00 | <0.01 | <0.01 | 0.03 | 0.01 | 0.67 | 0.87 | 0.62 | 0.03 | 0.65 | 0.85 | 0.54 | ||
1D | 7 | 1.00 | 1.00 | 1.00 | 0.04 | 1.00 | 1.00 | 1.00 | <0.01 | 0.03 | 0.02 | 0.04 | 0.73 | 0.04 | 0.01 | <0.01 | |
14 | 1.00 | 1.00 | 0.91 | 0.01 | 1.00 | 1.00 | 0.99 | <0.01 | 1.00 | 0.79 | 0.94 | 0.08 | 0.98 | 0.54 | 0.30 | ||
21 | 0.17 | 0.27 | 0.96 | 1.00 | 0.18 | 0.04 | 0.84 | 0.81 | 0.30 | 0.12 | 0.74 | 0.04 | 0.77 | 0.73 | 0.44 | ||
28 | 0.02 | 0.03 | 0.42 | 1.00 | 0.02 | <0.01 | 0.23 | 1.00 | 0.03 | 0.01 | 1.00 | 0.09 | 0.97 | 0.49 | 0.27 | ||
2D | 7 | 1.00 | 1.00 | 0.98 | 0.03 | 1.00 | 1.00 | 1.00 | <0.01 | 1.00 | 1.00 | 0.20 | 0.02 | 0.08 | 0.02 | <0.01 | |
14 | 1.00 | 1.00 | 0.90 | 0.01 | 1.00 | 1.00 | 0.98 | <0.01 | 1.00 | 1.00 | 0.10 | 0.01 | 1.00 | 0.52 | 0.29 | ||
21 | 0.39 | 0.55 | 1.00 | 0.99 | 0.42 | 0.12 | 0.98 | 0.51 | 0.60 | 0.29 | 1.00 | 0.97 | 0.45 | 0.27 | 0.67 | ||
28 | 0.01 | 0.01 | 0.23 | 1.00 | 0.01 | <0.01 | 0.11 | 1.00 | 0.01 | <0.01 | 0.99 | 1.00 | 0.01 | <0.01 | 0.86 |
Dose/ Time (Days) | p Values | ||||||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Control | 1/2D | D | 2D | ||||||||||||||
7 | 14 | 21 | 28 | 7 | 14 | 21 | 28 | 7 | 14 | 21 | 28 | 7 | 14 | 21 | 28 | ||
Control | 7 | <0.01 | <0.01 | <0.01 | 0.98 | 0.65 | <0.01 | 1.00 | 0.83 | <0.01 | <0.01 | 0.38 | 0.98 | <0.01 | <0.01 | 0.08 | |
14 | 0.02 | 0.99 | 0.65 | <0.01 | <0.01 | 0.89 | <0.01 | <0.01 | 0.23 | 0.87 | <0.01 | <0.01 | 0.08 | 0.99 | 0.01 | ||
21 | 0.08 | 0.55 | 0.11 | <0.01 | <0.01 | 1.00 | <0.01 | <0.01 | 0.86 | 1.00 | <0.01 | <0.01 | 0.55 | 0.48 | <0.01 | ||
28 | 0.09 | 0.52 | 0.97 | <0.01 | 0.38 | 0.06 | 0.02 | 0.23 | <0.01 | 0.06 | 0.36 | 0.03 | <0.01 | 1.00 | 0.87 | ||
1/2D | 7 | 0.03 | 0.87 | 0.66 | 0.63 | 0.04 | <0.01 | 0.25 | 0.08 | <0.01 | <0.01 | 0.01 | 0.16 | <0.01 | <0.01 | <0.01 | |
14 | 0.01 | 0.69 | 0.35 | 0.33 | 0.59 | <0.01 | 0.99 | 1.00 | <0.01 | <0.01 | 1.00 | 1.00 | <0.01 | 0.09 | 1.00 | ||
21 | <0.01 | 0.41 | 0.17 | 0.16 | 0.33 | 0.70 | <0.01 | <0.01 | 1.00 | 1.00 | <0.01 | <0.01 | 0.95 | 0.29 | <0.01 | ||
28 | 0.20 | 0.27 | 0.61 | 0.63 | 0.34 | 0.16 | 0.07 | 1.00 | <0.01 | <0.01 | 0.93 | 1.00 | <0.01 | <0.01 | 0.40 | ||
1D | 7 | 0.36 | 0.13 | 0.36 | 0.37 | 0.17 | 0.08 | 0.03 | 0.68 | <0.01 | <0.01 | 1.00 | 1.00 | <0.01 | <0.05 | 0.98 | |
14 | 0.01 | 0.57 | 0.27 | 0.26 | 0.48 | 0.88 | 0.82 | 0.12 | 0.05 | 1.00 | <0.01 | <0.01 | 1.00 | 0.03 | <0.01 | ||
21 | <0.01 | 0.46 | 0.18 | 0.17 | 0.37 | 0.80 | 0.86 | 0.07 | 0.02 | 0.93 | <0.01 | <0.01 | 0.96 | 0.26 | <0.01 | ||
28 | 0.07 | 0.61 | 0.92 | 0.90 | 0.73 | 0.39 | 0.20 | 0.55 | 0.31 | 0.31 | 0.22 | 0.98 | <0.01 | 0.07 | 1.00 | ||
2D | 7 | 0.43 | 0.10 | 0.29 | 0.30 | 0.13 | 0.06 | 0.02 | 0.58 | 0.89 | 0.04 | 0.02 | 0.25 | <0.01 | <0.01 | 0.55 | |
14 | 0.12 | 0.40 | 0.81 | 0.84 | 0.49 | 0.25 | 0.11 | 0.79 | 0.49 | 0.19 | 0.12 | 0.74 | 0.41 | 0.01 | <0.01 | ||
21 | 0.01 | 0.77 | 0.37 | 0.36 | 0.66 | 0.89 | 0.57 | 0.16 | 0.07 | 0.75 | 0.66 | 0.43 | 0.05 | 0.26 | 0.36 | ||
28 | 0.47 | 0.08 | 0.25 | 0.27 | 0.11 | <0.05 | 0.02 | 0.52 | 0.82 | 0.03 | 0.01 | 0.22 | 0.94 | 0.36 | 0.04 |
Dose/ Time (Days) | p Values | ||||||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Control | 1/2D | D | 2D | ||||||||||||||
7 | 14 | 21 | 28 | 7 | 14 | 21 | 28 | 7 | 14 | 21 | 28 | 7 | 14 | 21 | 28 | ||
Control | 7 | 0.97 | 1.00 | 0.10 | <0.01 | 1.00 | 0.99 | 0.11 | <0.01 | 1.00 | 0.98 | 0.07 | <0.01 | 1.00 | 0.99 | 0.11 | |
14 | 0.02 | 1.00 | 0.86 | <0.01 | 1.00 | 1.00 | 0.88 | <0.01 | 0.66 | 1.00 | 0.78 | <0.01 | 1.00 | 1.00 | 0.79 | ||
21 | <0.01 | 0.41 | 0.38 | <0.01 | 1.00 | 1.00 | 0.40 | <0.01 | 0.98 | 1.00 | 0.30 | <0.01 | 1.00 | 1.00 | 0.35 | ||
28 | 0.13 | 0.59 | 0.20 | <0.01 | 0.63 | 0.73 | 1.00 | <0.01 | 0.02 | 0.84 | 1.00 | <0.01 | 0.28 | 0.78 | 1.00 | ||
1/2D | 7 | 0.38 | 0.15 | 0.02 | 0.46 | <0.01 | <0.01 | <0.01 | 0.02 | <0.01 | <0.01 | <0.01 | <0.01 | <0.01 | <0.01 | <0.01 | |
14 | 0.03 | 0.91 | 0.35 | 0.66 | 0.19 | 1.00 | 0.65 | <0.01 | 0.99 | 1.00 | 0.53 | <0.01 | 1.00 | 1.00 | 0.55 | ||
21 | <0.01 | 0.15 | 0.53 | 0.07 | <0.01 | 0.12 | 0.76 | <0.01 | 0.80 | 1.00 | 0.63 | <0.01 | 1.00 | 1.00 | 0.66 | ||
28 | 0.28 | 0.22 | 0.04 | 0.57 | 0.84 | 0.26 | 0.01 | <0.01 | 0.02 | 0.86 | 1.00 | <0.01 | 0.30 | 0.80 | 1.00 | ||
1D | 7 | 0.65 | 0.11 | 0.02 | 0.33 | 0.75 | 0.13 | <0.01 | 0.62 | <0.01 | <0.01 | <0.01 | 0.99 | <0.01 | <0.01 | <0.01 | |
14 | 0.02 | 0.99 | 0.40 | 0.60 | 0.16 | 0.93 | 0.14 | 0.23 | 0.11 | 0.68 | 0.01 | <0.01 | 1.00 | 0.76 | 0.03 | ||
21 | <0.01 | 0.18 | 0.60 | 0.08 | 0.01 | 0.14 | 0.93 | 0.01 | <0.01 | 0.17 | 0.76 | <0.01 | 1.00 | 1.00 | 0.77 | ||
28 | 0.83 | 0.06 | 0.01 | 0.23 | 0.57 | 0.08 | <0.01 | 0.45 | 0.82 | 0.07 | <0.01 | <0.01 | 0.21 | 0.68 | 1.00 | ||
2D | 7 | 0.16 | 0.37 | 0.08 | 0.79 | 0.60 | 0.43 | 0.02 | 0.74 | 0.43 | 0.38 | 0.02 | 0.30 | <0.01 | <0.01 | <0.01 | |
14 | 0.01 | 0.64 | 0.72 | 0.34 | 0.06 | 0.57 | 0.33 | 0.09 | 0.04 | 0.63 | 0.38 | 0.02 | 0.17 | 1.00 | 0.26 | ||
21 | <0.01 | 0.26 | 0.76 | 0.12 | 0.01 | 0.21 | 0.76 | 0.02 | 0.01 | 0.25 | 0.83 | <0.01 | 0.04 | 0.50 | 0.71 | ||
28 | 0.37 | 0.16 | 0.03 | 0.47 | 0.98 | 0.20 | <0.01 | 0.86 | 0.73 | 0.17 | 0.01 | 0.55 | 0.62 | 0.06 | 0.01 |
Enzyme | Organism | ΔG (kcal/mol) | |||
---|---|---|---|---|---|
(R)-Flutriafol | Mean Value | (S)-Flutriafol | Mean Value | ||
Dehydrogenase | Clostridium beijerinckii | −8.41 | −8.48 | ||
Aspergillus fumigatus | −7.51 | −7.85 | −6.89 | −7.58 | |
Rhizobium leguminosarum | −7.63 | −7.38 | |||
Phosphatase | Bacillus subtilis | −7.54 | −7.75 | ||
Aspergillus niger | −7.22 | −7.36 | it does not bind to the active site | −7.45 | |
Rhizobium leguminosarum | −7.32 | −7.16 | |||
Catalase | Komagataella pastoris | −9.16 | −9.16 | −9.04 | −9.04 |
Enzyme | Ligand | Residues Associated with the Non-Covalent Interactions |
---|---|---|
Clostridium beijerinckii dehydrogenase | (R)-flutriafol | GLY176, ALA177, VAL178, GLY179, ARG200 |
(S)-flutriafol | THR38, ILE175, GLY176, ALA177, VAL178, TYR267, ILE345 | |
NADPH | THR38, SER39, ILE175, ALA176, VAL178, GLY179, SER199, ARG200, GLU247, ASN266, TYR267, LYS340 | |
Aspergillus fumigatus dehydrogenase | (R)-flutriafol | GLY44, PHE45, THR139GLN244 |
(S)-flutriafol | GLY44, PHE45, THR137, THR139, GLU140 | |
NADPH | GLY44, PHE45, GLN74, ASP77 (2), ASP199, ASN200, VAL238, THR242 | |
Rhizobium leguminosarum dehydrogenase | (R)-flutriafol | PRO161, TRP162, LYS186, SER240 |
(S)-flutriafol | TRP162, LYS186, ALA188, SER240 | |
NADPH | THR160, PRO161,LYS186, PRO187, SER240, GLU261 | |
Bacillus subtilis phosphatase | (R)-flutriafol | TYR66, TYR152, TYR153, ARG223, TYR226, LEU230, GLN263 |
(S)-flutriafol | - | |
Inhibitory peptide | TYR66, TYR152, TYR153, LYS155, GLN183, LEU187, ASP194, ARG223, TYR226 ASN227, SER260, GLN263, PHE266, TYR300, GLU303, ALA334, ASP335, ASP338 | |
Aspergillus niger phosphatase | (R)-flutriafol | ALA292, ASN296, LEU415, ASP417, TYR418, THR419, LEU432 |
NAG | ASN296, THR300, ASN439, LEU432 | |
Rhizobium leguminosarum phosphatase | (R)-flutriafol | TYR105, PHE138, ASN141 |
(S)-flutriafol | TYR105, LEU125, PHE138, ASN141, TYR215 | |
Calcium | ASP12, ASP324, HIS325 |
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Roman, D.-L.; Matica, M.A.; Boros, B.-V.; Vulpe, C.-B.; Isvoran, A. Evaluation of the Impact of Flutriafol on Soil Culturable Microorganisms and on Soil Enzymes Activity. Agriculture 2024, 14, 1445. https://doi.org/10.3390/agriculture14091445
Roman D-L, Matica MA, Boros B-V, Vulpe C-B, Isvoran A. Evaluation of the Impact of Flutriafol on Soil Culturable Microorganisms and on Soil Enzymes Activity. Agriculture. 2024; 14(9):1445. https://doi.org/10.3390/agriculture14091445
Chicago/Turabian StyleRoman, Diana-Larisa, Mariana Adina Matica, Bianca-Vanesa Boros, Constantina-Bianca Vulpe, and Adriana Isvoran. 2024. "Evaluation of the Impact of Flutriafol on Soil Culturable Microorganisms and on Soil Enzymes Activity" Agriculture 14, no. 9: 1445. https://doi.org/10.3390/agriculture14091445