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Fecal microbiota and bile acid interactions with systemic and adipose tissue metabolism in diet-induced weight loss of obese postmenopausal women

Fecal microbiota and bile acid interactions with systemic and adipose tissue metabolism in diet-induced weight loss of obese postmenopausal women
Fecal microbiota and bile acid interactions with systemic and adipose tissue metabolism in diet-induced weight loss of obese postmenopausal women

BACKGROUND: Microbiota and bile acids in the gastrointestinal tract profoundly alter systemic metabolic processes. In obese subjects, gradual weight loss ameliorates adipose tissue inflammation and related systemic changes. We assessed how rapid weight loss due to a very low calorie diet (VLCD) affects the fecal microbiome and fecal bile acid composition, and their interactions with the plasma metabolome and subcutaneous adipose tissue inflammation in obesity.

METHODS: We performed a prospective cohort study of VLCD-induced weight loss of 10% in ten grades 2-3 obese postmenopausal women in a metabolic unit. Baseline and post weight loss evaluation included fasting plasma analyzed by mass spectrometry, adipose tissue transcription by RNA sequencing, stool 16S rRNA sequencing for fecal microbiota, fecal bile acids by mass spectrometry, and urinary metabolic phenotyping by 1H-NMR spectroscopy. Outcome measures included mixed model correlations between changes in fecal microbiota and bile acid composition with changes in plasma metabolite and adipose tissue gene expression pathways.

RESULTS: Alterations in the urinary metabolic phenotype following VLCD-induced weight loss were consistent with starvation ketosis, protein sparing, and disruptions to the functional status of the gut microbiota. We show that the core microbiome was preserved during VLCD-induced weight loss, but with changes in several groups of bacterial taxa with functional implications. UniFrac analysis showed overall parallel shifts in community structure, corresponding to reduced abundance of the genus Roseburia and increased Christensenellaceae;g__ (unknown genus). Imputed microbial functions showed changes in fat and carbohydrate metabolism. A significant fall in fecal total bile acid concentration and reduced deconjugation and 7-α-dihydroxylation were accompanied by significant changes in several bacterial taxa. Individual bile acids in feces correlated with amino acid, purine, and lipid metabolic pathways in plasma. Furthermore, several fecal bile acids and bacterial species correlated with altered gene expression pathways in adipose tissue.

CONCLUSIONS: VLCD dietary intervention in obese women changed the composition of several fecal microbial populations while preserving the core fecal microbiome. Changes in individual microbial taxa and their functions correlated with variations in the plasma metabolome, fecal bile acid composition, and adipose tissue transcriptome. Trial Registration ClinicalTrials.gov NCT01699906, 4-Oct-2012, Retrospectively registered. URL- https://clinicaltrials.gov/ct2/show/NCT01699906.

Adipose Tissue/metabolism, Adult, Aged, Bile Acids and Salts/chemistry, Caloric Restriction, Carbohydrate Metabolism, Diet, Reducing, Feces/microbiology, Female, Gene Expression Profiling, Gene Expression Regulation, Humans, Inflammation, Ketosis/urine, Metabolomics, Middle Aged, Obesity/microbiology, Phenotype, Postmenopause, Prospective Studies, RNA, Ribosomal, 16S/metabolism, Sequence Analysis, RNA, Weight Loss
1479-5876
1-17
Alemán, José O.
061a64d8-71e8-4b7f-97f6-1b7708d65e19
Bokulich, Nicholas A.
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Swann, Jonathan R.
7c11a66b-f4b8-4dbf-aa17-ad8b0561b85c
Walker, Jeanne M.
111a8fb0-3376-4cc3-b2ab-f899feb9bcf3
De Rosa, Joel Correa
a7ea9a9f-42e4-4221-b31b-570e87d5d5b4
Battaglia, Thomas
c6fb20c9-de75-4296-9eee-706f6081bee2
Costabile, Adele
2f54d3f0-8414-4844-8296-e97f6097e09e
Pechlivanis, Alexandros
ed3ffe12-0d36-4225-af8b-dfbfdd4b9e6f
Liang, Yupu
68a3a3da-0825-4d24-a503-0ff828a2ca1b
Breslow, Jan L.
d4c3a5d8-0446-40b2-95fc-b30b10567886
Blaser, Martin J.
fe0adcf2-132c-4ba1-9286-445588baf54a
Holt, Peter R.
59c2f200-c61d-412c-81ef-af39fa43e29d
Alemán, José O.
061a64d8-71e8-4b7f-97f6-1b7708d65e19
Bokulich, Nicholas A.
f7aa085f-30e2-4430-b008-b7b4a73a9dc6
Swann, Jonathan R.
7c11a66b-f4b8-4dbf-aa17-ad8b0561b85c
Walker, Jeanne M.
111a8fb0-3376-4cc3-b2ab-f899feb9bcf3
De Rosa, Joel Correa
a7ea9a9f-42e4-4221-b31b-570e87d5d5b4
Battaglia, Thomas
c6fb20c9-de75-4296-9eee-706f6081bee2
Costabile, Adele
2f54d3f0-8414-4844-8296-e97f6097e09e
Pechlivanis, Alexandros
ed3ffe12-0d36-4225-af8b-dfbfdd4b9e6f
Liang, Yupu
68a3a3da-0825-4d24-a503-0ff828a2ca1b
Breslow, Jan L.
d4c3a5d8-0446-40b2-95fc-b30b10567886
Blaser, Martin J.
fe0adcf2-132c-4ba1-9286-445588baf54a
Holt, Peter R.
59c2f200-c61d-412c-81ef-af39fa43e29d

Alemán, José O., Bokulich, Nicholas A., Swann, Jonathan R., Walker, Jeanne M., De Rosa, Joel Correa, Battaglia, Thomas, Costabile, Adele, Pechlivanis, Alexandros, Liang, Yupu, Breslow, Jan L., Blaser, Martin J. and Holt, Peter R. (2018) Fecal microbiota and bile acid interactions with systemic and adipose tissue metabolism in diet-induced weight loss of obese postmenopausal women. Journal of Translational Medicine, 16 (1), 1-17, [244]. (doi:10.1186/s12967-018-1619-z).

Record type: Article

Abstract

BACKGROUND: Microbiota and bile acids in the gastrointestinal tract profoundly alter systemic metabolic processes. In obese subjects, gradual weight loss ameliorates adipose tissue inflammation and related systemic changes. We assessed how rapid weight loss due to a very low calorie diet (VLCD) affects the fecal microbiome and fecal bile acid composition, and their interactions with the plasma metabolome and subcutaneous adipose tissue inflammation in obesity.

METHODS: We performed a prospective cohort study of VLCD-induced weight loss of 10% in ten grades 2-3 obese postmenopausal women in a metabolic unit. Baseline and post weight loss evaluation included fasting plasma analyzed by mass spectrometry, adipose tissue transcription by RNA sequencing, stool 16S rRNA sequencing for fecal microbiota, fecal bile acids by mass spectrometry, and urinary metabolic phenotyping by 1H-NMR spectroscopy. Outcome measures included mixed model correlations between changes in fecal microbiota and bile acid composition with changes in plasma metabolite and adipose tissue gene expression pathways.

RESULTS: Alterations in the urinary metabolic phenotype following VLCD-induced weight loss were consistent with starvation ketosis, protein sparing, and disruptions to the functional status of the gut microbiota. We show that the core microbiome was preserved during VLCD-induced weight loss, but with changes in several groups of bacterial taxa with functional implications. UniFrac analysis showed overall parallel shifts in community structure, corresponding to reduced abundance of the genus Roseburia and increased Christensenellaceae;g__ (unknown genus). Imputed microbial functions showed changes in fat and carbohydrate metabolism. A significant fall in fecal total bile acid concentration and reduced deconjugation and 7-α-dihydroxylation were accompanied by significant changes in several bacterial taxa. Individual bile acids in feces correlated with amino acid, purine, and lipid metabolic pathways in plasma. Furthermore, several fecal bile acids and bacterial species correlated with altered gene expression pathways in adipose tissue.

CONCLUSIONS: VLCD dietary intervention in obese women changed the composition of several fecal microbial populations while preserving the core fecal microbiome. Changes in individual microbial taxa and their functions correlated with variations in the plasma metabolome, fecal bile acid composition, and adipose tissue transcriptome. Trial Registration ClinicalTrials.gov NCT01699906, 4-Oct-2012, Retrospectively registered. URL- https://clinicaltrials.gov/ct2/show/NCT01699906.

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Accepted/In Press date: 25 August 2018
Published date: 3 September 2018
Keywords: Adipose Tissue/metabolism, Adult, Aged, Bile Acids and Salts/chemistry, Caloric Restriction, Carbohydrate Metabolism, Diet, Reducing, Feces/microbiology, Female, Gene Expression Profiling, Gene Expression Regulation, Humans, Inflammation, Ketosis/urine, Metabolomics, Middle Aged, Obesity/microbiology, Phenotype, Postmenopause, Prospective Studies, RNA, Ribosomal, 16S/metabolism, Sequence Analysis, RNA, Weight Loss

Identifiers

Local EPrints ID: 440789
URI: http://eprints.soton.ac.uk/id/eprint/440789
ISSN: 1479-5876
PURE UUID: 408ef624-e0c8-4622-b811-273639bca646
ORCID for Jonathan R. Swann: ORCID iD orcid.org/0000-0002-6485-4529

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Date deposited: 18 May 2020 16:53
Last modified: 17 Mar 2024 04:00

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Contributors

Author: José O. Alemán
Author: Nicholas A. Bokulich
Author: Jeanne M. Walker
Author: Joel Correa De Rosa
Author: Thomas Battaglia
Author: Adele Costabile
Author: Alexandros Pechlivanis
Author: Yupu Liang
Author: Jan L. Breslow
Author: Martin J. Blaser
Author: Peter R. Holt

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