The effects of consuming white button mushroom-Agaricus Bisporus-on the brain and liver metabolome using a targeted metabolomic analysis

Authors: Solano-Aguilar, Gloria; Lakshman, Sukla; Jang, Saebyeol; GUPTA, RICHI - George Mason University; Molokin, Aleksey; Schroeder, Steven - Steve; GILLEVET, PATRICK - George Mason University; Urban, Joseph

Submitted to: Metabolites
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/11/2021
Publication Date: 11/15/2021
Citation: Solano-Aguilar, G.I., Lakshman, S., Jang, S., Gupta, R., Molokin, A., Schroeder, S.G., Gillevet, P.M., Urban Jr., J.F. 2021. The effects of consuming white button mushroom Agaricus bisporus on the brain and liver metabolome using a targeted metabolomic analysis. Metabolites. 11(11):779. https://doi.org/10.3390/metabo11110779.
DOI: https://doi.org/10.3390/metabo11110779

Interpretive Summary: This study shows the effect of feeding white button mushroom (WBM) on the abundance and composition of metabolites in liver and brain of pigs and its association with bacteria previously identified to respond to a diet supplemented with mushroom. Thirty-one six-week -old pigs were fed a grower diet alone or supplemented with either three or six servings of freeze-dried WBM for six weeks. The metabolites within the liver and two sections of the brain: hippocampus and cortex were measured using targeted liquid chromatography-mass spectrometry (LC-MS) combined with an analysis that compared the chemical structure of the metabolites. Changes in tissue metabolites were correlated with changes in bacteria within the fecal microbiome. Results indicated that consumption of diets supplemented with WBM can differentially modulate metabolites in the liver, brain cortex and hippocampus of healthy pigs. Within the glycerophospholipids class of metabolites, there was an increase in alkyl-acyl-phosphatidylcholines (PC-O 40:3) in the hippocampus of pigs supplemented with six servings of WBM compared to pigs fed the control diet. A broader change in glycerophospholipids and sphingolipids was detected in the liver with a reduction in several phosphatidylcholines, alkyl-acyl-phosphatidylcholines, lyso-alkyl-phosphatidylcholines, sphingomyelin, and ceramides in pigs fed both WBM supplemented diets with an increase in amino acids known to serve primarily as precursors of neurotransmitters in the cortex in pigs fed the 6 servings WBM diet. Metabolomic changes in the brain and liver were positively correlated with increased abundance of bacteria within the families Cryomorphaceae, Lachnospiraceae, Flammeovirgaceae and Ruminococcaceae which had previously been shown to respond to WBM in the diet suggesting dietary interventions with WBM can also positively impact host metabolic function.

Technical Abstract: A targeted metabolomic analysis was performed on tissues derived from pigs fed diets supplemented with white button mushrooms (WBM) to determine the effect on the liver and brain metabolome associated with bacterial taxa previously identified as responsive to WBM in the diet. Thirty-one six-week -old pigs were fed a grower diet alone or supplemented with either three or six servings of freeze-dried WBM for six weeks. The liver and brain metabolomes were measured using targeted liquid chromatography-mass spectrometry (LC-MS) combined with chemical similarity enrichment analysis (ChemRICH) and correlated to changes in the composition of the fecal microbiome. Results indicated that consumption of diets supplemented with WBM can differentially modulate metabolites in the liver, brain cortex and hippocampus of healthy pigs. Within the glycerophospholipids, there was an increase in alkyl-acyl-phosphatidylcholines (PC-O 40:3) in the hippocampus of pigs supplemented with six servings of WBM compared to pigs fed the control diet. A broader change in glycerophospholipids and sphingolipids was detected in the liver with a reduction in several phosphatidylcholines, alkyl-acyl-phosphatidylcholines, lyso-alkyl-phosphatidylcholines, sphingomyelin, and ceramides in pigs fed both WBM supplemented diets with an increase in amino acids known to serve primarily as precursors of neurotransmitters in the cortex in pigs fed the 6 servings WBM diet. Metabolomic changes in the brain and liver were positively correlated with increased abundance of bacteria within the families Cryomorphaceae, Lachnospiraceae, Flammeovirgaceae and Ruminococcaceae which had previously been shown to respond to WBM in the diet suggesting dietary interventions with WBM can also positively impact host metabolic function.