Gut microbiome and metabolome in a non-human primate model of chronic excessive alcohol drinking

Abstract A relationship between the gut microbiome and alcohol use disorder has been suggested. Excessive alcohol use produces changes in the fecal microbiome and metabolome in both rodents and humans. Yet, these changes can be observed only in a subgroup of the studied populations, and reversal doe...

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Autores principales:	Daria Piacentino, Silvia Grant-Beurmann, Carlotta Vizioli, Xiaobai Li, Catherine F. Moore, Victor Ruiz-Rodado, Mary R. Lee, Paule V. Joseph, Claire M. Fraser, Elise M. Weerts, Lorenzo Leggio
Formato:	article
Lenguaje:	EN
Publicado:	Nature Publishing Group 2021
Materias:	Neurosciences. Biological psychiatry. Neuropsychiatry RC321-571
Acceso en línea:	https://doaj.org/article/be343213178043c89709f48da8c119e8
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spelling	oai:doaj.org-article:be343213178043c89709f48da8c119e82021-12-05T12:07:47ZGut microbiome and metabolome in a non-human primate model of chronic excessive alcohol drinking10.1038/s41398-021-01728-62158-3188https://doaj.org/article/be343213178043c89709f48da8c119e82021-12-01T00:00:00Zhttps://doi.org/10.1038/s41398-021-01728-6https://doaj.org/toc/2158-3188Abstract A relationship between the gut microbiome and alcohol use disorder has been suggested. Excessive alcohol use produces changes in the fecal microbiome and metabolome in both rodents and humans. Yet, these changes can be observed only in a subgroup of the studied populations, and reversal does not always occur after abstinence. We aimed to analyze fecal microbial composition and function in a translationally relevant baboon model of chronic heavy drinking that also meets binge criteria (drinking too much, too fast, and too often), i.e., alcohol ~1 g/kg and blood alcohol levels (BALs) ≥ 0.08 g/dL in a 2-hour period, daily, for years. We compared three groups of male baboons (Papio anubis): L = Long-term alcohol drinking group (12.1 years); S = Short-term alcohol drinking group (2.7 years); and C = Control group, drinking a non-alcoholic reinforcer (Tang®) (8.2 years). Fecal collection took place during 3 days of Drinking (D), followed by a short period (3 days) of Abstinence (A). Fecal microbial alpha- and beta-diversity were significantly lower in L vs. S and C (p’s < 0.05). Members of the commensal families Lachnospiraceae and Prevotellaceae showed a relative decrease, whereas the opportunistic pathogen Streptococcus genus showed a relative increase in L vs. S and C (p’s < 0.05). Microbiota-related metabolites of aromatic amino acids, tricarboxylic acid cycle, and pentose increased in L vs. S and C (FDR-corrected p < 0.01), with the latter two suggesting high energy metabolism and enhanced glycolysis in the gut lumen in response to alcohol. Consistent with the long-term alcohol exposure, mucosal damage and oxidative stress markers (N-acetylated amino acids, 2-hydroxybutyrate, and metabolites of the methionine cycle) increased in L vs. S and C (FDR-corrected p < 0.01). Overall, S showed few differences vs. C, possibly due to the long-term, chronic alcohol exposure needed to alter the normal gut microbiota. In the three groups, the fecal microbiome barely differed between conditions D and A, whereas the metabolome shifted in the transition from condition D to A. In conclusion, changes in the fecal microbiome and metabolome occur after significant long-term excessive drinking and are only partially affected by acute forced abstinence from alcohol. These results provide novel information on the relationship between the fecal microbiome and metabolome in a controlled experimental setting and using a unique non-human primate model of chronic excessive alcohol drinking.Daria PiacentinoSilvia Grant-BeurmannCarlotta VizioliXiaobai LiCatherine F. MooreVictor Ruiz-RodadoMary R. LeePaule V. JosephClaire M. FraserElise M. WeertsLorenzo LeggioNature Publishing GrouparticleNeurosciences. Biological psychiatry. NeuropsychiatryRC321-571ENTranslational Psychiatry, Vol 11, Iss 1, Pp 1-15 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Neurosciences. Biological psychiatry. Neuropsychiatry RC321-571
spellingShingle	Neurosciences. Biological psychiatry. Neuropsychiatry RC321-571 Daria Piacentino Silvia Grant-Beurmann Carlotta Vizioli Xiaobai Li Catherine F. Moore Victor Ruiz-Rodado Mary R. Lee Paule V. Joseph Claire M. Fraser Elise M. Weerts Lorenzo Leggio Gut microbiome and metabolome in a non-human primate model of chronic excessive alcohol drinking
description	Abstract A relationship between the gut microbiome and alcohol use disorder has been suggested. Excessive alcohol use produces changes in the fecal microbiome and metabolome in both rodents and humans. Yet, these changes can be observed only in a subgroup of the studied populations, and reversal does not always occur after abstinence. We aimed to analyze fecal microbial composition and function in a translationally relevant baboon model of chronic heavy drinking that also meets binge criteria (drinking too much, too fast, and too often), i.e., alcohol ~1 g/kg and blood alcohol levels (BALs) ≥ 0.08 g/dL in a 2-hour period, daily, for years. We compared three groups of male baboons (Papio anubis): L = Long-term alcohol drinking group (12.1 years); S = Short-term alcohol drinking group (2.7 years); and C = Control group, drinking a non-alcoholic reinforcer (Tang®) (8.2 years). Fecal collection took place during 3 days of Drinking (D), followed by a short period (3 days) of Abstinence (A). Fecal microbial alpha- and beta-diversity were significantly lower in L vs. S and C (p’s < 0.05). Members of the commensal families Lachnospiraceae and Prevotellaceae showed a relative decrease, whereas the opportunistic pathogen Streptococcus genus showed a relative increase in L vs. S and C (p’s < 0.05). Microbiota-related metabolites of aromatic amino acids, tricarboxylic acid cycle, and pentose increased in L vs. S and C (FDR-corrected p < 0.01), with the latter two suggesting high energy metabolism and enhanced glycolysis in the gut lumen in response to alcohol. Consistent with the long-term alcohol exposure, mucosal damage and oxidative stress markers (N-acetylated amino acids, 2-hydroxybutyrate, and metabolites of the methionine cycle) increased in L vs. S and C (FDR-corrected p < 0.01). Overall, S showed few differences vs. C, possibly due to the long-term, chronic alcohol exposure needed to alter the normal gut microbiota. In the three groups, the fecal microbiome barely differed between conditions D and A, whereas the metabolome shifted in the transition from condition D to A. In conclusion, changes in the fecal microbiome and metabolome occur after significant long-term excessive drinking and are only partially affected by acute forced abstinence from alcohol. These results provide novel information on the relationship between the fecal microbiome and metabolome in a controlled experimental setting and using a unique non-human primate model of chronic excessive alcohol drinking.
format	article
author	Daria Piacentino Silvia Grant-Beurmann Carlotta Vizioli Xiaobai Li Catherine F. Moore Victor Ruiz-Rodado Mary R. Lee Paule V. Joseph Claire M. Fraser Elise M. Weerts Lorenzo Leggio
author_facet	Daria Piacentino Silvia Grant-Beurmann Carlotta Vizioli Xiaobai Li Catherine F. Moore Victor Ruiz-Rodado Mary R. Lee Paule V. Joseph Claire M. Fraser Elise M. Weerts Lorenzo Leggio
author_sort	Daria Piacentino
title	Gut microbiome and metabolome in a non-human primate model of chronic excessive alcohol drinking
title_short	Gut microbiome and metabolome in a non-human primate model of chronic excessive alcohol drinking
title_full	Gut microbiome and metabolome in a non-human primate model of chronic excessive alcohol drinking
title_fullStr	Gut microbiome and metabolome in a non-human primate model of chronic excessive alcohol drinking
title_full_unstemmed	Gut microbiome and metabolome in a non-human primate model of chronic excessive alcohol drinking
title_sort	gut microbiome and metabolome in a non-human primate model of chronic excessive alcohol drinking
publisher	Nature Publishing Group
publishDate	2021
url	https://doaj.org/article/be343213178043c89709f48da8c119e8
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Gut microbiome and metabolome in a non-human primate model of chronic excessive alcohol drinking

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