The Microbiome, Epigenome, and Diet in Adults with Obesity during Behavioral Weight Loss

Obesity has been linked to the gut microbiome, epigenome, and diet, yet these factors have not been studied together during obesity treatment. Our objective was to evaluate associations among gut microbiota (MB), DNA methylation (DNAme), and diet prior to and during a behavioral weight loss interven...

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Main Authors: Emily B. Hill, Iain R. Konigsberg, Diana Ir, Daniel N. Frank, Purevsuren Jambal, Elizabeth M. Litkowski, Ethan M. Lange, Leslie A. Lange, Danielle M. Ostendorf, Jared J. Scorsone, Liza Wayland, Kristen Bing, Paul S. MacLean, Edward L. Melanson, Daniel H. Bessesen, Victoria A. Catenacci, Maggie A. Stanislawski, Sarah J. Borengasser
Format: Article
Language:English
Published: MDPI AG 2023-08-01
Series:Nutrients
Subjects:
Online Access:https://www.mdpi.com/2072-6643/15/16/3588
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author Emily B. Hill
Iain R. Konigsberg
Diana Ir
Daniel N. Frank
Purevsuren Jambal
Elizabeth M. Litkowski
Ethan M. Lange
Leslie A. Lange
Danielle M. Ostendorf
Jared J. Scorsone
Liza Wayland
Kristen Bing
Paul S. MacLean
Edward L. Melanson
Daniel H. Bessesen
Victoria A. Catenacci
Maggie A. Stanislawski
Sarah J. Borengasser
author_facet Emily B. Hill
Iain R. Konigsberg
Diana Ir
Daniel N. Frank
Purevsuren Jambal
Elizabeth M. Litkowski
Ethan M. Lange
Leslie A. Lange
Danielle M. Ostendorf
Jared J. Scorsone
Liza Wayland
Kristen Bing
Paul S. MacLean
Edward L. Melanson
Daniel H. Bessesen
Victoria A. Catenacci
Maggie A. Stanislawski
Sarah J. Borengasser
author_sort Emily B. Hill
collection DOAJ
description Obesity has been linked to the gut microbiome, epigenome, and diet, yet these factors have not been studied together during obesity treatment. Our objective was to evaluate associations among gut microbiota (MB), DNA methylation (DNAme), and diet prior to and during a behavioral weight loss intervention. Adults (<i>n</i> = 47, age 40.9 ± 9.7 years, body mass index (BMI) 33.5 ± 4.5 kg/m<sup>2</sup>, 77% female) with data collected at baseline (BL) and 3 months (3 m) were included. Fecal MB was assessed via 16S sequencing and whole blood DNAme via the Infinium EPIC array. Food group and nutrient intakes and Healthy Eating Index (HEI) scores were calculated from 7-day diet records. Linear models were used to test for the effect of taxa relative abundance on DNAme and diet cross-sectionally at each time point, adjusting for confounders and a false discovery rate of 5%. Mean weight loss was 6.2 ± 3.9% at 3 m. At BL, one MB taxon, <i>Ruminiclostridium</i>, was associated with DNAme of the genes <i>COL20A1</i> (r = 0.651, <i>p</i> = 0.029), <i>COL18A1</i> (r = 0.578, <i>p</i> = 0.044), and <i>NT5E</i> (r = 0.365, <i>p</i> = 0.043). At 3 m, there were 14 unique MB:DNAme associations, such as <i>Akkermansia</i> with DNAme of <i>GUSB</i> (r = −0.585, <i>p</i> = 0.003), <i>CRYL1</i> (r = −0.419, <i>p</i> = 0.007), <i>C9</i> (r = −0.439, <i>p</i> = 0.019), and <i>GMDS</i> (r = −0.559, <i>p</i> = 0.046). Among taxa associated with DNAme, no significant relationships were seen with dietary intakes of relevant nutrients, food groups, or HEI scores. Our findings indicate that microbes linked to mucin degradation, short-chain fatty acid production, and body weight are associated with DNAme of phenotypically relevant genes. These relationships offer an initial understanding of the possible routes by which alterations in gut MB may influence metabolism during weight loss.
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spelling doaj.art-12eb4929d4de40b7a62c9ba0582b84c12023-11-19T02:30:13ZengMDPI AGNutrients2072-66432023-08-011516358810.3390/nu15163588The Microbiome, Epigenome, and Diet in Adults with Obesity during Behavioral Weight LossEmily B. Hill0Iain R. Konigsberg1Diana Ir2Daniel N. Frank3Purevsuren Jambal4Elizabeth M. Litkowski5Ethan M. Lange6Leslie A. Lange7Danielle M. Ostendorf8Jared J. Scorsone9Liza Wayland10Kristen Bing11Paul S. MacLean12Edward L. Melanson13Daniel H. Bessesen14Victoria A. Catenacci15Maggie A. Stanislawski16Sarah J. Borengasser17Section of Nutrition, Department of Pediatrics, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USADepartment of Biomedical Informatics, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USADivision of Infectious Diseases, Department of Medicine, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USADivision of Infectious Diseases, Department of Medicine, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USASection of Nutrition, Department of Pediatrics, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USADepartment of Biomedical Informatics, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USADepartment of Biomedical Informatics, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USADepartment of Biomedical Informatics, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USADivision of Endocrinology, Metabolism, and Diabetes, Department of Medicine, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USAAnschutz Health and Wellness Center, Department of Medicine, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USADivision of Endocrinology, Metabolism, and Diabetes, Department of Medicine, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USAAnschutz Health and Wellness Center, Department of Medicine, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USADivision of Endocrinology, Metabolism, and Diabetes, Department of Medicine, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USADivision of Endocrinology, Metabolism, and Diabetes, Department of Medicine, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USADivision of Endocrinology, Metabolism, and Diabetes, Department of Medicine, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USADivision of Endocrinology, Metabolism, and Diabetes, Department of Medicine, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USADepartment of Biomedical Informatics, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USASection of Nutrition, Department of Pediatrics, University of Colorado Anschutz Medical Campus, Aurora, CO 80045, USAObesity has been linked to the gut microbiome, epigenome, and diet, yet these factors have not been studied together during obesity treatment. Our objective was to evaluate associations among gut microbiota (MB), DNA methylation (DNAme), and diet prior to and during a behavioral weight loss intervention. Adults (<i>n</i> = 47, age 40.9 ± 9.7 years, body mass index (BMI) 33.5 ± 4.5 kg/m<sup>2</sup>, 77% female) with data collected at baseline (BL) and 3 months (3 m) were included. Fecal MB was assessed via 16S sequencing and whole blood DNAme via the Infinium EPIC array. Food group and nutrient intakes and Healthy Eating Index (HEI) scores were calculated from 7-day diet records. Linear models were used to test for the effect of taxa relative abundance on DNAme and diet cross-sectionally at each time point, adjusting for confounders and a false discovery rate of 5%. Mean weight loss was 6.2 ± 3.9% at 3 m. At BL, one MB taxon, <i>Ruminiclostridium</i>, was associated with DNAme of the genes <i>COL20A1</i> (r = 0.651, <i>p</i> = 0.029), <i>COL18A1</i> (r = 0.578, <i>p</i> = 0.044), and <i>NT5E</i> (r = 0.365, <i>p</i> = 0.043). At 3 m, there were 14 unique MB:DNAme associations, such as <i>Akkermansia</i> with DNAme of <i>GUSB</i> (r = −0.585, <i>p</i> = 0.003), <i>CRYL1</i> (r = −0.419, <i>p</i> = 0.007), <i>C9</i> (r = −0.439, <i>p</i> = 0.019), and <i>GMDS</i> (r = −0.559, <i>p</i> = 0.046). Among taxa associated with DNAme, no significant relationships were seen with dietary intakes of relevant nutrients, food groups, or HEI scores. Our findings indicate that microbes linked to mucin degradation, short-chain fatty acid production, and body weight are associated with DNAme of phenotypically relevant genes. These relationships offer an initial understanding of the possible routes by which alterations in gut MB may influence metabolism during weight loss.https://www.mdpi.com/2072-6643/15/16/3588DNA methylationepigeneticsgut microbiomedietlifestyleobesity
spellingShingle Emily B. Hill
Iain R. Konigsberg
Diana Ir
Daniel N. Frank
Purevsuren Jambal
Elizabeth M. Litkowski
Ethan M. Lange
Leslie A. Lange
Danielle M. Ostendorf
Jared J. Scorsone
Liza Wayland
Kristen Bing
Paul S. MacLean
Edward L. Melanson
Daniel H. Bessesen
Victoria A. Catenacci
Maggie A. Stanislawski
Sarah J. Borengasser
The Microbiome, Epigenome, and Diet in Adults with Obesity during Behavioral Weight Loss
Nutrients
DNA methylation
epigenetics
gut microbiome
diet
lifestyle
obesity
title The Microbiome, Epigenome, and Diet in Adults with Obesity during Behavioral Weight Loss
title_full The Microbiome, Epigenome, and Diet in Adults with Obesity during Behavioral Weight Loss
title_fullStr The Microbiome, Epigenome, and Diet in Adults with Obesity during Behavioral Weight Loss
title_full_unstemmed The Microbiome, Epigenome, and Diet in Adults with Obesity during Behavioral Weight Loss
title_short The Microbiome, Epigenome, and Diet in Adults with Obesity during Behavioral Weight Loss
title_sort microbiome epigenome and diet in adults with obesity during behavioral weight loss
topic DNA methylation
epigenetics
gut microbiome
diet
lifestyle
obesity
url https://www.mdpi.com/2072-6643/15/16/3588
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