Response of the gut microbiome and metabolome to dietary fiber in healthy dogs

ABSTRACT Dietary fiber confers multiple health benefits originating from the expansion of beneficial gut microbial activity. However, very few studies have established the metabolic consequences of interactions among specific fibers, microbiome composition, and function in either human or representa...

Full description

Saved in:
Bibliographic Details
Main Authors: Amrisha Bhosle, Matthew I. Jackson, Aaron M. Walsh, Eric A. Franzosa, Dayakar V. Badri, Curtis Huttenhower
Format: Article
Language:English
Published: American Society for Microbiology 2025-01-01
Series:mSystems
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/msystems.00452-24
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1832592153288638464
author Amrisha Bhosle
Matthew I. Jackson
Aaron M. Walsh
Eric A. Franzosa
Dayakar V. Badri
Curtis Huttenhower
author_facet Amrisha Bhosle
Matthew I. Jackson
Aaron M. Walsh
Eric A. Franzosa
Dayakar V. Badri
Curtis Huttenhower
author_sort Amrisha Bhosle
collection DOAJ
description ABSTRACT Dietary fiber confers multiple health benefits originating from the expansion of beneficial gut microbial activity. However, very few studies have established the metabolic consequences of interactions among specific fibers, microbiome composition, and function in either human or representative animal models. In a study design reflective of realistic population dietary variation, fecal metagenomic and metabolomic profiles were analyzed from healthy dogs fed 12 test foods containing different fiber sources and quantities (5–13% as-fed basis). Taxa and functions were identified whose abundances were associated either with overall fiber intake or with specific fiber compositions. Fourteen microbial species were significantly enriched in response to ≥1 specific fiber source; enrichment of fiber-derived metabolites was more pronounced in response to these fiber sources. Positively associated fecal metabolites, including short-chain fatty acids, acylglycerols, fiber bound sugars, and polyphenols, co-occurred with microbes enriched in specific food groups. Critically, the specific metabolite pools responsive to differential fiber intake were dependent on differences both in individual microbial community membership and in overall ecological configuration. This helps to explain, for the first time, differences in microbiome-diet associations observed in companion animal epidemiology. Thus, our study corroborates findings in human cohorts and reinforces the role of personalized microbiomes even in seemingly phenotypically homogeneous subjects.IMPORTANCEConsumption of dietary fiber changes the composition of the gut microbiome and, to a larger extent, the associated metabolites. Production of health-relevant metabolites such as short-chain fatty acids from fiber depends both on the consumption of a specific fiber and on the enrichment of beneficial metabolite-producing species in response to it. Even in a seemingly homogeneous population, the benefit received from fiber consumption is personalized and emphasizes specific fiber-microbe-host interactions. These observations are relevant for both population-wide and personalized nutrition applications.
format Article
id doaj-art-76469be4098d4d7ba5e8c3452318e3ee
institution Kabale University
issn 2379-5077
language English
publishDate 2025-01-01
publisher American Society for Microbiology
record_format Article
series mSystems
spelling doaj-art-76469be4098d4d7ba5e8c3452318e3ee2025-01-21T14:00:28ZengAmerican Society for MicrobiologymSystems2379-50772025-01-0110110.1128/msystems.00452-24Response of the gut microbiome and metabolome to dietary fiber in healthy dogsAmrisha Bhosle0Matthew I. Jackson1Aaron M. Walsh2Eric A. Franzosa3Dayakar V. Badri4Curtis Huttenhower5Infectious Disease and Microbiome Program, Broad Institute of MIT and Harvard, Cambridge, Massachusetts, USAHill’s Pet Nutrition Inc., Topeka, Kansas, USADepartment of Biostatistics, Harvard T. H. Chan School of Public Health, Boston, Massachusetts, USAInfectious Disease and Microbiome Program, Broad Institute of MIT and Harvard, Cambridge, Massachusetts, USAHill’s Pet Nutrition Inc., Topeka, Kansas, USAInfectious Disease and Microbiome Program, Broad Institute of MIT and Harvard, Cambridge, Massachusetts, USAABSTRACT Dietary fiber confers multiple health benefits originating from the expansion of beneficial gut microbial activity. However, very few studies have established the metabolic consequences of interactions among specific fibers, microbiome composition, and function in either human or representative animal models. In a study design reflective of realistic population dietary variation, fecal metagenomic and metabolomic profiles were analyzed from healthy dogs fed 12 test foods containing different fiber sources and quantities (5–13% as-fed basis). Taxa and functions were identified whose abundances were associated either with overall fiber intake or with specific fiber compositions. Fourteen microbial species were significantly enriched in response to ≥1 specific fiber source; enrichment of fiber-derived metabolites was more pronounced in response to these fiber sources. Positively associated fecal metabolites, including short-chain fatty acids, acylglycerols, fiber bound sugars, and polyphenols, co-occurred with microbes enriched in specific food groups. Critically, the specific metabolite pools responsive to differential fiber intake were dependent on differences both in individual microbial community membership and in overall ecological configuration. This helps to explain, for the first time, differences in microbiome-diet associations observed in companion animal epidemiology. Thus, our study corroborates findings in human cohorts and reinforces the role of personalized microbiomes even in seemingly phenotypically homogeneous subjects.IMPORTANCEConsumption of dietary fiber changes the composition of the gut microbiome and, to a larger extent, the associated metabolites. Production of health-relevant metabolites such as short-chain fatty acids from fiber depends both on the consumption of a specific fiber and on the enrichment of beneficial metabolite-producing species in response to it. Even in a seemingly homogeneous population, the benefit received from fiber consumption is personalized and emphasizes specific fiber-microbe-host interactions. These observations are relevant for both population-wide and personalized nutrition applications.https://journals.asm.org/doi/10.1128/msystems.00452-24caninedietary fibermetabolomegut microbiomepersonalized nutrition
spellingShingle Amrisha Bhosle
Matthew I. Jackson
Aaron M. Walsh
Eric A. Franzosa
Dayakar V. Badri
Curtis Huttenhower
Response of the gut microbiome and metabolome to dietary fiber in healthy dogs
mSystems
canine
dietary fiber
metabolome
gut microbiome
personalized nutrition
title Response of the gut microbiome and metabolome to dietary fiber in healthy dogs
title_full Response of the gut microbiome and metabolome to dietary fiber in healthy dogs
title_fullStr Response of the gut microbiome and metabolome to dietary fiber in healthy dogs
title_full_unstemmed Response of the gut microbiome and metabolome to dietary fiber in healthy dogs
title_short Response of the gut microbiome and metabolome to dietary fiber in healthy dogs
title_sort response of the gut microbiome and metabolome to dietary fiber in healthy dogs
topic canine
dietary fiber
metabolome
gut microbiome
personalized nutrition
url https://journals.asm.org/doi/10.1128/msystems.00452-24
work_keys_str_mv AT amrishabhosle responseofthegutmicrobiomeandmetabolometodietaryfiberinhealthydogs
AT matthewijackson responseofthegutmicrobiomeandmetabolometodietaryfiberinhealthydogs
AT aaronmwalsh responseofthegutmicrobiomeandmetabolometodietaryfiberinhealthydogs
AT ericafranzosa responseofthegutmicrobiomeandmetabolometodietaryfiberinhealthydogs
AT dayakarvbadri responseofthegutmicrobiomeandmetabolometodietaryfiberinhealthydogs
AT curtishuttenhower responseofthegutmicrobiomeandmetabolometodietaryfiberinhealthydogs