The Effects of Consuming White Button Mushroom Agaricus bisporus on the Brain and Liver Metabolome Using a Targeted Metabolomic Analysis
Abstract
:1. Introduction
2. Results
2.1. Metabolome Profile Analysis
2.2. Metabolic Analysis by ChemRICH
2.3. Associations of Metabolites with Fecal Microbiota
2.4. RNA Sequencing of Brain
3. Discussion
4. Materials and Methods
4.1. Ethics Statement
4.2. Diet Formulation and Tissue Sample Collection
4.3. Targeted Metabolomic Analysis
4.4. Statistical Analysis of Metabolomic Data
4.5. RNA Sequencing and Mapping
4.6. RNA-Seq Data Analysis
4.7. Differentially Expressed Genes-Real Time PCR Validation
4.8. 16 S rDNA Amplicon Multi-Tag Sequencing Data and Metabolite Correlations
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Metabolite Class | Liver | Cortex | Hippocampus |
---|---|---|---|
Acyl-carnitines (55) * | 3 | 3 | 3 |
Amino acids (21) | 17 | 17 | 17 |
Biogenic Amines (21) | 11 | 7 | 7 |
Cholesterol Esters (14) | 5 | 5 | 5 |
Diglycerides (18) | 6 | 2 | 2 |
Triglycerides (42) | 1 | 1 | 1 |
Phosphatidylcholine (172) | 92 | 93 | 96 |
Lyso-phosphatidylcholine (24) | 8 | 8 | 8 |
Sphingomyelins (31) | 21 | 16 | 17 |
Ceramides (9) | 2 | 1 | 1 |
Monosaccharides (1) | 1 | 1 | 1 |
total (408) | 167 | 154 | 158 |
Mean Rank | 3 Serv. vs. Control | 6 Serv. vs. Control | 6 Serv. vs. 3 Serv. | Cortex Vip | |||||||
---|---|---|---|---|---|---|---|---|---|---|---|
Metabolite | Class | Control | 3 Servings | 6 Servings | FC | FDR | FC | FDR | FC | FDR | |
Arg | Aminoacids | 13.11 * | 10.33 | 18.56 | 0.94 | 0.340 | 1.20 | 0.141 | 1.27 | 0.141 | 1.93 |
Gln | Aminoacids | 10.56 | 13.33 | 18.11 | 1.12 | 0.730 | 1.16 | 0.056 | 1.03 | 0.581 | 1.54 |
Met | Aminoacids | 11.11 | 12.33 | 18.56 | 0.99 | 1.000 | 1.23 | 0.073 | 1.24 | 0.285 | 1.47 |
Thr | Aminoacids | 8.61 | 15.50 | 17.89 | 1.11 | 0.183 | 1.35 | 0.017 | 1.22 | 0.730 | 1.41 |
Taurine | Biogenic Amines | 12.56 | 10.72 | 18.72 | 0.86 | 0.596 | 1.12 | 0.140 | 1.31 | 0.140 | 1.58 |
DG (42:2) | Glycerides | 9.78 | 13.06 | 19.17 | 1.07 | 0.401 | 1.18 | 0.045 | 1.10 | 0.170 | 2.05 |
PC (29:1) | Glycerophospholipids | 10.72 | 12.83 | 18.44 | 1.10 | 0.562 | 1.22 | 0.154 | 1.11 | 0.200 | 1.80 |
LPC (20:4) | Glycerophospholipids | 10.17 | 13.28 | 18.56 | 1.04 | 0.401 | 1.13 | 0.102 | 1.09 | 0.242 | 1.74 |
PC-O (40:4) | Glycerophospholipids | 10.89 | 13.17 | 17.94 | 1.61 | 0.436 | 1.86 | 0.217 | 1.15 | 0.217 | 1.74 |
PC-O (34:3) | Glycerophospholipids | 11.11 | 12.78 | 18.11 | 1.17 | 0.507 | 1.38 | 0.183 | 1.18 | 0.183 | 1.64 |
PC-O (38:5) | Glycerophospholipids | 13.22 | 11.44 | 17.33 | 0.92 | 0.605 | 1.15 | 0.387 | 1.25 | 0.387 | 1.57 |
PC-O (40:5) | Glycerophospholipids | 12.00 | 12.11 | 17.89 | 1.07 | 1.000 | 1.13 | 0.200 | 1.06 | 0.200 | 1.49 |
PC (33:5) | Glycerophospholipids | 10.11 | 13.94 | 17.94 | 1.07 | 0.331 | 1.14 | 0.125 | 1.06 | 0.331 | 1.46 |
PC (34:2) | Glycerophospholipids | 11.17 | 13.06 | 17.78 | 0.99 | 0.627 | 1.08 | 0.278 | 1.09 | 0.324 | 1.46 |
PC (31:1) | Glycerophospholipids | 12.72 | 11.33 | 17.94 | 0.99 | 0.626 | 1.04 | 0.200 | 1.05 | 0.200 | 1.45 |
SM (38:2) | Sphingolipids | 11.11 | 12.22 | 18.67 | 1.02 | 0.796 | 1.18 | 0.141 | 1.15 | 0.141 | 2.14 |
SM (32:1) | Sphingolipids | 10.11 | 12.89 | 19.00 | 1.03 | 0.387 | 1.49 | 0.094 | 1.44 | 0.115 | 2.12 |
SM (34:2) | Sphingolipids | 11.89 | 11.56 | 18.56 | 1.08 | 0.931 | 1.28 | 0.115 | 1.19 | 0.115 | 1.54 |
- | - | Mean Ranks | 3 Serv. vs. Control | 6 Serv. vs. Control | 6 Serv. vs. 3 Serv. | Hippocampus VIP | |||||
---|---|---|---|---|---|---|---|---|---|---|---|
Metabolite | Class | Control | 3 Serv. | 6 Serv. | FC | FDR | FC | FDR | FC | FDR | |
Taurine | Biogenic Amines | 12 * | 11.56 | 18.44 | 0.82 | 0.863 | 1.26 | 0.141 | 1.54 | 0.141 | 1.48 |
CE (19:2) | Cholesterol Esters | 16.17 | 9.56 | 16.28 | 0.85 | 0.153 | 1.06 | 0.931 | 1.24 | 0.153 | 1.86 |
DG (38:5) | Glycerides | 14.67 | 9.78 | 17.56 | 0.79 | 0.285 | 1.64 | 0.436 | 2.08 | 0.151 | 1.83 |
PC-O (40:3) | Glycerophospholipids | 11.33 | 10.44 | 20.22 | 0.85 | 0.48 | 2.08 | 0.008 | 2.46 | 0.063 | 2.24 |
PC (39:3) | Glycerophospholipids | 14.39 | 10.22 | 17.39 | 0.86 | 0.376 | 1.00 | 0.401 | 1.17 | 0.232 | 1.96 |
PC (41:4) | Glycerophospholipids | 13.56 | 10.78 | 17.67 | 0.78 | 0.436 | 1.25 | 0.387 | 1.60 | 0.282 | 1.80 |
PC (39:4) | Glycerophospholipids | 14.89 | 10.83 | 16.28 | 0.89 | 0.465 | 1.05 | 0.757 | 1.17 | 0.465 | 1.67 |
PC (33:2) | Glycerophospholipids | 11.94 | 11.89 | 18.17 | 1.03 | 1.000 | 1.51 | 0.183 | 1.47 | 0.183 | 1.66 |
PC (42:4) | Glycerophospholipids | 17.22 | 10.17 | 14.61 | 0.83 | 0.19 | 0.97 | 0.536 | 1.17 | 0.404 | 1.65 |
PC (36:3) | Glycerophospholipids | 14.67 | 10.56 | 16.78 | 0.80 | 0.426 | 0.99 | 0.594 | 1.24 | 0.333 | 1.61 |
PC (37:1) | Glycerophospholipids | 13.22 | 11.61 | 17.17 | 0.51 | 0.666 | 1.27 | 0.434 | 2.51 | 0.434 | 1.61 |
PC (38:2) | Glycerophospholipids | 14.44 | 10.22 | 17.33 | 0.74 | 0.35 | 1.05 | 0.401 | 1.41 | 0.255 | 1.52 |
PC (37:2) | Glycerophospholipids | 14.33 | 10.89 | 16.78 | 0.76 | 0.436 | 1.17 | 0.436 | 1.54 | 0.436 | 1.50 |
PC (36:1) | Glycerophospholipids | 13.94 | 11.22 | 16.83 | 0.80 | 0.387 | 1.07 | 0.387 | 1.34 | 0.387 | 1.49 |
PC (39:5) | Glycerophospholipids | 20.72 | 9.72 | 11.56 | 0.84 | 0.009 | 0.88 | 0.032 | 1.05 | 0.723 | 1.35 |
PC (42:6) | Glycerophospholipids | 19.89 | 11.33 | 10.78 | 0.82 | 0.024 | 0.75 | 0.077 | 0.92 | 0.595 | 1.00 |
PC-O (33:3) | Glycerophospholipids | 13.22 | 11.00 | 17.78 | 0.87 | 0.436 | 1.58 | 0.242 | 1.83 | 0.242 | 1.48 |
PC (31:1) | Glycerophospholipids | 12.61 | 12.67 | 16.72 | 0.99 | 1.000 | 1.06 | 0.510 | 1.07 | 0.510 | 1.46 |
PC-O (33:4) | Glycerophospholipids | 13.22 | 11.44 | 17.33 | 0.85 | 0.596 | 1.13 | 0.387 | 1.34 | 0.387 | 1.45 |
SM (38:2) | Sphingolipids | 13.11 | 11.00 | 17.89 | 0.99 | 0.536 | 1.33 | 0.277 | 1.34 | 0.277 | 1.87 |
SM (41:2) | Sphingolipids | 12.44 | 11.28 | 18.28 | 0.74 | 0.791 | 1.38 | 0.200 | 1.87 | 0.200 | 1.81 |
SM (40:2) | Sphingolipids | 12.11 | 11.39 | 18.50 | 0.92 | 0.73 | 1.58 | 0.153 | 1.71 | 0.153 | 1.74 |
SM (43:2) | Sphingolipids | 13.00 | 11.22 | 17.78 | 0.95 | 0.605 | 1.44 | 0.285 | 1.51 | 0.285 | 1.69 |
SM (42:2) | Sphingolipids | 13.00 | 10.89 | 18.11 | 0.84 | 0.536 | 1.48 | 0.236 | 1.77 | 0.231 | 1.68 |
- | - | Mean Rank | 3 Serv. vs. Control | 6 Serv. vs. Control | 6 Serv. vs. 3 Serv. | Liver VIP- | |||||
---|---|---|---|---|---|---|---|---|---|---|---|
Metabolite | Class | Control | 3 Serv. | 6 Serv. | FC | FDR | FC | FDR | FC | FDR | |
AC (4:0-OH) | Acylcarnitines | 10.25 * | 16.17 | 13.72 | 1.12 | 0.275 | 1.13 | 0.627 | 1.01 | 0.627 | 1.54 |
Serotonin | Biogenic Amines | 9.19 | 20.89 | 9.94 | 2.40 | 0.007 | 1.09 | 0.700 | 0.45 | 0.001 | 2.07 |
CE (22:5) | Cholesterol Esters | 17.63 | 11.44 | 11.89 | 0.86 | 0.204 | 0.86 | 0.204 | 1.00 | 0.930 | 1.49 |
DG (36:2) | Glycerides | 18.00 | 9.61 | 13.39 | 0.60 | 0.162 | 0.88 | 0.222 | 1.48 | 0.222 | 1.67 |
PC (31:1) | Glycerophospholipids | 20.00 | 9.33 | 11.89 | 0.61 | 0.024 | 0.62 | 0.031 | 1.03 | 0.427 | 2.31 |
PC (35:1) | Glycerophospholipids | 19.31 | 9.39 | 12.44 | 0.64 | 0.017 | 0.82 | 0.125 | 1.28 | 0.453 | 2.26 |
PC-O (33:4) | Glycerophospholipids | 19.38 | 8.56 | 13.22 | 0.73 | 0.017 | 0.77 | 0.112 | 1.05 | 0.161 | 2.23 |
PC-O (35:4) | Glycerophospholipids | 19.69 | 9.78 | 11.72 | 0.46 | 0.029 | 0.62 | 0.047 | 1.33 | 0.574 | 2.18 |
PC (46:2) | Glycerophospholipids | 19.63 | 9.78 | 11.78 | 0.39 | 0.034 | 0.47 | 0.034 | 1.19 | 0.418 | 2.16 |
LPC (15:0) | Glycerophospholipids | 19.25 | 10.67 | 11.22 | 0.67 | 0.045 | 0.83 | 0.045 | 1.23 | 0.860 | 2.14 |
PC (39:3) | Glycerophospholipids | 18.63 | 8.00 | 14.44 | 0.72 | 0.024 | 0.85 | 0.228 | 1.18 | 0.095 | 2.12 |
PC (33:1) | Glycerophospholipids | 18.88 | 9.44 | 12.78 | 0.66 | 0.024 | 0.74 | 0.209 | 1.12 | 0.436 | 2.07 |
PC (35:4) | Glycerophospholipids | 20.50 | 10.00 | 10.78 | 0.86 | 0.014 | 0.85 | 0.021 | 0.99 | 0.930 | 1.98 |
PC-O (33:3) | Glycerophospholipids | 17.88 | 10.11 | 13.00 | 0.72 | 0.139 | 0.75 | 0.300 | 1.04 | 0.436 | 1.91 |
PC (37:1) | Glycerophospholipids | 19.00 | 10.67 | 11.44 | 0.75 | 0.070 | 0.84 | 0.070 | 1.11 | 0.863 | 1.86 |
PC (32:6) | Glycerophospholipids | 7.19 | 15.89 | 16.72 | 1.61 | 0.027 | 1.44 | 0.027 | 0.89 | 0.791 | 1.84 |
PC (38:2) | Glycerophospholipids | 8.00 | 17.72 | 14.17 | 2.00 | 0.037 | 1.86 | 0.152 | 0.93 | 0.331 | 1.81 |
PC (31:0) | Glycerophospholipids | 17.50 | 11.78 | 11.67 | 0.97 | 0.290 | 0.87 | 0.275 | 0.89 | 0.931 | 1.65 |
PC (33:0) | Glycerophospholipids | 17.63 | 10.28 | 13.06 | 0.79 | 0.178 | 0.92 | 0.354 | 1.17 | 0.453 | 1.64 |
PC (30:0) | Glycerophospholipids | 17.88 | 11.33 | 11.78 | 0.84 | 0.171 | 0.76 | 0.171 | 0.90 | 0.931 | 1.60 |
PC (32:1) | Glycerophospholipids | 17.81 | 10.39 | 12.78 | 0.77 | 0.103 | 0.89 | 0.402 | 1.16 | 0.659 | 1.48 |
SM (43:1) | Sphingolipids | 20.50 | 9.67 | 11.11 | 0.61 | 0.008 | 0.64 | 0.008 | 1.06 | 0.605 | 2.43 |
SM (42:1) | Sphingolipids | 20.38 | 11.17 | 9.72 | 0.72 | 0.018 | 0.63 | 0.018 | 0.88 | 0.666 | 2.16 |
Cer (42:1) | Sphingolipids | 20.13 | 8.78 | 12.33 | 0.61 | 0.007 | 0.78 | 0.041 | 1.28 | 0.297 | 2.16 |
SM (41:1) | Sphingolipids | 17.88 | 11.78 | 11.33 | 0.92 | 0.171 | 0.86 | 0.171 | 0.93 | 0.931 | 1.81 |
Cer (42:2) | Sphingolipids | 17.63 | 9.89 | 13.44 | 0.65 | 0.223 | 0.75 | 0.258 | 1.17 | 0.258 | 1.58 |
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Solano-Aguilar, G.I.; Lakshman, S.; Jang, S.; Gupta, R.; Molokin, A.; Schroeder, S.G.; Gillevet, P.M.; Urban, J.F., Jr. The Effects of Consuming White Button Mushroom Agaricus bisporus on the Brain and Liver Metabolome Using a Targeted Metabolomic Analysis. Metabolites 2021, 11, 779. https://0-doi-org.brum.beds.ac.uk/10.3390/metabo11110779
Solano-Aguilar GI, Lakshman S, Jang S, Gupta R, Molokin A, Schroeder SG, Gillevet PM, Urban JF Jr. The Effects of Consuming White Button Mushroom Agaricus bisporus on the Brain and Liver Metabolome Using a Targeted Metabolomic Analysis. Metabolites. 2021; 11(11):779. https://0-doi-org.brum.beds.ac.uk/10.3390/metabo11110779
Chicago/Turabian StyleSolano-Aguilar, Gloria I., Sukla Lakshman, Saebyeol Jang, Richi Gupta, Aleksey Molokin, Steven G. Schroeder, Patrick M. Gillevet, and Joseph F. Urban, Jr. 2021. "The Effects of Consuming White Button Mushroom Agaricus bisporus on the Brain and Liver Metabolome Using a Targeted Metabolomic Analysis" Metabolites 11, no. 11: 779. https://0-doi-org.brum.beds.ac.uk/10.3390/metabo11110779