The gut-brain axis mediates bacterial driven modulation of reward signaling

Kim, Jiyoung S.; Williams, Keith; Kirkland, Rebecca A.; Schade, Ruth; Freeman, Kimberly G.; Cawthon, Carolina R.; Rautmann, Allison W.; Smith, Jessica M.; Edwards, Gaylen L.; Glenn, Travis C.; Holmes, Philip V.; Lartigue, Guillaume de; Serre, Claire B. de La

doi:10.1016/j.molmet.2023.101764

Cited by 6 publications

(15 citation statements)

References 87 publications

(168 reference statements)

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“…It also expresses many microbial metabolite receptors 38,39 and connects to feeding-related brain regions such as the ARH 40 and striatum 41,42 through multisynaptic pathways. Through selective ablation of gut-innervating vagal neurons, a role for vagal nerve signaling has also been shown for bacterial modulation of high fat diet preference 9 . However, most literature studying bacterial modulation of host diet preference has focused on preference for palatable diets and reward-related brain regions such as the nucleus accumbens [8][9][10] .…”

Section: Discussionmentioning

confidence: 99%

“…Through selective ablation of gut-innervating vagal neurons, a role for vagal nerve signaling has also been shown for bacterial modulation of high fat diet preference 9 . However, most literature studying bacterial modulation of host diet preference has focused on preference for palatable diets and reward-related brain regions such as the nucleus accumbens [8][9][10] . The role of bacterial modulation of homeostatic feeding circuits in the ARH through the vagus nerve remains unclear.…”

Section: Discussionmentioning

confidence: 99%

“…The results suggest that the strength of host diet association may depend on the efficiency of bacterial fructan degradation and amount of its fermentation products, such as the SCFA acetate, to the host. B. thetaiotaomicron grows robustly on its fermentable LD, reaching over 10 9 colony forming units by hour 12 ( Fig. 1c , Extended Data Fig.…”

Section: Discussionmentioning

confidence: 99%

“…The gut microbiome has the capacity to modify host appetite and preference for diets that vary in macronutrient composition [5][6][7][8][9][10]13,14 . To determine whether differential fructan utilization by gut bacteria alters host preference for diets that vary only in fructan source, we began by selecting B. ovatus and B. thetaiotaomicron based on their reported selectivity in degrading inulin and levan 20 , respectively, which are fructans that differ only in their glycosidic linkages (Fig.…”

Section: Colonization With Fructan-utilizing Bacteria Promotes Host P...mentioning

confidence: 99%

“…In mice, colonization with microbiota from wild rodents with different foraging strategies conferred differential food preferences, where those colonized with herbivoreassociated microbiota preferred diets with a higher protein to carbohydrate ratio diet than those colonized with omnivore-and carnivore-associated microbiota 7 . Similarly, transplanting microbiota from obese donor mice into lean recipient mice lowered preference for high fat diets, which was correlated with deficits in dopamine signaling in the nucleus accumbens 8,9 . Conversely, treating mice with antibiotics to deplete gut bacteria led them to overconsume palatable high-sucrose diets 10 .…”

Section: Introductionmentioning

confidence: 99%

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Complex carbohydrate utilization by gut bacteria modulates host food preference

Yu,

Son,

Chandra

et al. 2024

Preprint

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The gut microbiota interacts directly with dietary nutrients and has the ability to modify host feeding behavior, but the underlying mechanisms remain poorly understood. Select gut bacteria digest complex carbohydrates that are non-digestible by the host and liberate metabolites that serve as additional energy sources and pleiotropic signaling molecules. Here we use a gnotobiotic mouse model to examine how differential fructose polysaccharide metabolism by commensal gut bacteria influences host preference for diets containing these carbohydrates.Bacteroides thetaiotaomicronandBacteroides ovatusselectively ferment fructans with different glycosidic linkages:B. thetaiotaomicronferments levan with β2-6 linkages, whereasB. ovatusferments inulin with β2-1 linkages. Since inulin and levan are both fructose polymers, inulin and levan diet have similar perceptual salience to mice. We find that mice colonized withB. thetaiotaomicronprefer the non-fermentable inulin diet, while mice colonized withB. ovatusprefer the non-fermentable levan diet. Knockout of bacterial fructan utilization genes abrogates this preference, whereas swapping the fermentation ability ofB. thetaiotaomicronto inulin confers host preference for the levan diet. Bacterial fructan fermentation and host behavioral preference for the non-fermentable fructan are associated with increased neuronal activation in the arcuate nucleus of the hypothalamus, a key brain region for appetite regulation. These results reveal that selective nutrient metabolism by gut bacteria contributes to host associative learning of dietary preference, and further informs fundamental understanding of the biological determinants of food choice.

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