Gut microbiota link dietary fiber intake and short-chain fatty acid metabolism with eating behavior

Evelyn Medawar, Sven-Bastiaan Haange, Ulrike Rolle-Kampczyk, Beatrice Engelmann, Arne Dietrich, Ronja Thieleking, Charlotte Wiegank, Charlotte Fries, Annette Horstmann, Arno Villringer, Martin von Bergen, Wiebke Fenske, A Veronica Witte, Evelyn Medawar, Sven-Bastiaan Haange, Ulrike Rolle-Kampczyk, Beatrice Engelmann, Arne Dietrich, Ronja Thieleking, Charlotte Wiegank, Charlotte Fries, Annette Horstmann, Arno Villringer, Martin von Bergen, Wiebke Fenske, A Veronica Witte

Abstract

The gut microbiome has been speculated to modulate feeding behavior through multiple factors, including short-chain fatty acids (SCFA). Evidence on this relationship in humans is however lacking. We aimed to explore if specific bacterial genera relate to eating behavior, diet, and SCFA in adults. Moreover, we tested whether eating-related microbiota relate to treatment success in patients after Roux-en-Y gastric bypass (RYGB). Anthropometrics, dietary fiber intake, eating behavior, 16S-rRNA-derived microbiota, and fecal and serum SCFA were correlated in young overweight adults (n = 27 (9 F), 21-36 years, BMI 25-31 kg/m2). Correlated genera were compared in RYGB (n = 23 (16 F), 41-70 years, BMI 25-62 kg/m2) and control patients (n = 17 (11 F), 26-69 years, BMI 25-48 kg/m2). In young adults, 7 bacteria genera, i.e., Alistipes, Blautia, Clostridiales cluster XVIII, Gemmiger, Roseburia, Ruminococcus, and Streptococcus, correlated with healthier eating behavior, while 5 genera, i.e., Clostridiales cluster IV and XIVb, Collinsella, Fusicatenibacter, and Parabacteroides, correlated with unhealthier eating (all | r | > 0.4, FDR-corrected p < 0.05). Some of these genera including Parabacteroides related to fiber intake and SCFA, and to weight status and treatment response in overweight/obese patients. In this exploratory analysis, specific bacterial genera, particularly Parabacteroides, were associated with weight status and eating behavior in two small, independent and well-characterized cross-sectional samples. These preliminary findings suggest two groups of presumably beneficial and unfavorable genera that relate to eating behavior and weight status, and indicate that dietary fiber and SCFA metabolism may modify these relationships. Larger interventional studies are needed to distinguish correlation from causation.

Trial registration: ClinicalTrials.gov NCT03829189.

Conflict of interest statement

The authors declare no competing interests.

© 2021. The Author(s).

Figures

Fig. 1. Microbiota profiling of two cross-sectional…
Fig. 1. Microbiota profiling of two cross-sectional cohorts.
A Relative abundances of phyla per subject across sample of young, overweight adults (sample 1). Sorted by Firmicutes abundance. B Relative abundances of family per subject across sample of young, overweight adults (sample 1). C Relative abundances of phyla per group for overweight and obese adults and good and bad responders after RYGB (sample 2). Colors are as in panel A. D Relative abundances of family per group for overweight and obese adults and good and bad responders after RYGB (sample 2). Colors are as in panel B.
Fig. 2. Pearson’s correlations between eating behavior…
Fig. 2. Pearson’s correlations between eating behavior traits (TFEQ and hunger ratings) or health indicators and bacterial genera in overweight adults (all | r | > 0.42, all p-FDR < 0.05; sample 1).
A inversely health-related genera (blue), B health-related genera (yellow), C Collinsella and body fat mass (black), and D Streptococcus and mean systolic blood pressure (black).
Fig. 3. Habitual dietary fiber intake is…
Fig. 3. Habitual dietary fiber intake is associated with bacterial genera, body fat mass and eating traits.
Pearson’s correlations shown for inversely health-related genera (blue) (A, B), health-related genera (yellow) (C), body fat mass (black) (D), and eating trait disinhibition (TFEQ) (black) (E) (Pearson’s correlation all 0.75 < |r | > 0.58, all p-FDR < 0.05; sample 1 n = 27).
Fig. 4. SCFA levels in feces and…
Fig. 4. SCFA levels in feces and serum are associated with eating traits and body fat mass in overweight adults (sample 1).
Pearson’s correlations shown for fecal SCFA levels and eating trait cognitive restraint (TFEQ) (r = 0.50, p-FDR = 0.014) (A) and serum SCFA levels with body fat mass for acetate (B) and butyrate (C) (all r > −0.43, all p-FDR < 0.04).
Fig. 5. Sumscore of inversely health-related genera…
Fig. 5. Sumscore of inversely health-related genera is positively associated with eating traits (TFEQ).
Pearson’s correlations shown for microbial genera abundance sumscore for inversely health-related genera with respect to eating behavior outcomes from TFEQ and hunger ratings shown for A) cognitive restraint (r = 0.59, p-uncorr = 0.001) B) disinhibition (r = 0.65, p-uncorr < 0.001) C) hunger score D) 10 min-postprandial hunger E) 40 min-postprandial hunger and F) 65 min-postprandial hunger. Data from sample 1, all p-uncorrected.
Fig. 6. Differences in relative bacterial genera…
Fig. 6. Differences in relative bacterial genera abundance across groups of overweight, obese and post-RYGB adults in sample 2.
For A inversely health-related (blue), B positively related genera (yellow), C negative (blue), and D positive sumscores of all related genera (yellow) detected in sample 1. E Correlation of negative genera sumscore and/or Parabacteroides abundance with eating behavior and/or weight loss after RYGB surgery (green: good responders; red: bad responders). RYGB, Roux-en-Y gastric bypass. Mean + SD.

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