The gut microbiota is a major environmental contributor to host physiology and impacts feeding behavior


Herein, we reveal that the gut microbiota reduces feeding induced in response to various palatable foods in mice. We find the gut microbiota diminishes the incentive salience of high-sucrose pellets and regulates activity in reward-related brain regions.

Gut community profiling exposed microbial taxa associated with feeding suppression, and S24-7 family members and L. johnsonii were sufficient to reduce binge intake in an antibiotic-treatment model of overconsumption.

We found that microbiota-depleted mice overconsumed high-sucrose pellets, a HFD, and Ensure, suggesting our observations may generalize to other rewarding foods. Indeed, a recent report has demonstrated an antibiotic-induced increase in binge-like consumption of a high-fat high-sugar diet in mice.9

Although these sweet and fat stimuli model the processed diets contributing to disease in current Western populations,71 their composite nature limits our ability to draw conclusions about specific dietary properties required for microbiota-dependent changes in feeding. Targeted experiments involving foods with controlled levels of sweetness and fat, coupled with sensory pathway intervention, are needed to define these relationships.

Pertinently, two-bottle tests reveal GF mice overconsume sucrose solutions and fat emulsions and differentially express lingual fat-detection proteins compared with SPF controls.35,72

We observed microbiota-dependent changes in neural activity in the VTA and NAc, regions associated with hedonic feeding,2,3,15 in line with reports that microbiota perturbations may affect brain activity.73,74,75 Central regulators of palatable food intake, including dopamine, brain-derived neurotrophic factor, and endocannabinoids, differ in GF mice compared with mice with intact microbiotas76,77,78 and may regulate reward pathways that influence microbiota-mediated effects on palatable food consumption. Future research will explore specific molecular pathways linking the gut microbiota to mesolimbic brain activity.

Microbes from the S24-7 family and L. johnsonii are sufficient to suppress high-sucrose pellet intake in our model system, compared with treatment with A. muciniphila. Intriguingly, a strain of Bacteroides uniformis, of the same phylogenetic order as S24-7, can suppress binge eating in mice, and multiple species of Lactobacillus are reported to affect metabolism and feeding.10,79,80,81 A next stage of this research will define the mechanisms required for gut microbes to suppress palatable food consumption.

Altered gut microbiome profiles have been associated with human eating disorders, including anorexia nervosa and binge-eating disorder,82,83,84,85,86 as well as in rodent studies of palatable food intake, dietary preference, and eating disorder models.9,10,11,87,88,89

Our findings contribute new insights to growing evidence for functional gut microbiota modulation of host feeding behavior and identify candidate species for further study.10,12,13

Phenotypic correlations between feeding behavior traits in this study are similar to the results previously reported by Fernández et al. [14]. In agreement with Rauw et al. [36] and Carcò et al. [37], we observed an increase in both the feeding rate and feed consumption of pigs with age, most likely due to their increased physical capacity. As expected, we observed different feeding patterns between breeds. We found that Large White pigs had a lower feeding rate than Duroc and Landrace pigs during the first two periods. In contrast, Fernández et al. [14] found that Duroc had lowest feeding rate of the three breeds, defining them as “slow eaters”. Variations in feeding behaviors among rooms or pens for growing pigs were noticed in this study. It is expected that with only one Feeder equipped per pen, social ranks in group-housed pigs may lead to competition at feeding and result in a discrepancy in feeding behavior across pens [38].

First proposed by Difford et al. [34], estimation of microbiability has recently become a popular approach to quantify the proportion of variation in host phenotypes explained by the microbial composition in agricultural animal species. Difford et al. [34] reported that the ruminal microbiota composition was responsible for 15% of the total phenotypic variation in CH4 emissions of dairy cows. Wen et al. [39] indicated that the duodenal and cecal microbiota explained 24% and 21% of fat deposition variation in chicken, respectively.

Moreover, Vollmar et at. [40] reported that the variations in the gut microbiota were associated with 9%, 18%, and 27% of variations in the feed intake, daily gain, feed per gain ratio in Japanese Quail, respectively. Our microbiability estimates ranged from 0.09 to 0.31, which suggested that the gut microbiota was associated with a small to moderate amount of variation in host feeding behavior among animals. In this study, breed effects on microbiability were discovered.

Differences in the microbiability estimates between Duroc and Large White pigs suggest that the gut microbial composition may differ in predicting the host phenotype in populations with diverse genetic backgrounds. Furthermore, our findings show that the gut microbial composition of pigs at the finishing stage (T3) is more informative in explaining the variations in feeding behavior than at the start of the growth period (T1).

The differences in the microbiability estimates across time points could be explained by several factors. For example, if all microbial samples had been collected at a uniform time point (i.e., the midpoint) within each feeding behavior measurement period, we might have seen fewer variances in the microbiability. In addition, transitions in the diet and environment prior to our first sampling may have contributed to differences in the microbiability between growth stages. We also observed variations in the microbiability estimates across feeding behavior traits, with the highest values for average daily feed intake, ranging from 0.17 to 0.31, which are similar to the estimate of 0.16 for feed intake of Pietrain sows at the slaughter age estimated by Camarinha-Silva et al. [32]. To the best of our knowledge, our study is the first one to estimate the microbiability for feeder occupation time, feeding rate, and number of visits to the feeder in multiple breeds at three time points during the growth in swine. These findings suggest that host genetics and age may have an impact on microbiability for different traits in pigs, but more research is needed to confirm the findings in different populations.

Previous studies have suggested that the gut microbial composition varies among individuals due to breed and age in pigs [15, 16, 23]. In this study, the identified ASVs associated with feeding behavior were also breed-specific and stage-specific during the growing to finishing period, with a small part of ASVs shared among breeds or sampling time points. At the last sampling time point (158 days of age), the greatest number of ASVs were found associated with feeding behavior across breeds compared to the previous two sampling time points (73 and 123 days of age). This might be due to the relative higher alpha diversity measured by the Shannon Index and greater number of clusters in the gut microbiota at 158 days compared to early time points in all three breeds, as described in our previous study [23].

Among the 40 ASVs positively associated with feeding behavior, more than half of the ones associated with feed intake, feeding rate, and feeder occupation time were assigned to Lachnospiraceae family in Firmicutes phylum. Similarly, Cox et al. [41] identified four ASVs in Lachnospiraceae family that exhibited greater abundances in people with good appetite than people with poor appetite by comparing their gut microbial composition. At the genus level, two ASVs robust in positive associations with the daily feeder occupation time in multiple breeds and time points were annotated to Marvinbryantia and Dorea.

The remaining identified ASVs positively associated with the daily feeder occupation time were mainly annotated to Blautia and Ruminococcaceae_UCG-014. Interestingly, these microbes have been found correlated to complex host behaviors, such as stressor-induced behavior and depressive-like behavior in human and animal models [42–45]. Shifts in the abundance of Blautia [43], Dorea [42], and Marvinbryantia [45] were observed in stressed and depressed mice. Similarly, reduction in the abundance of Ruminococcaceae_UCG-014 was linked to the development of anxiety-like behaviors in humans [44]. The genus Prevotella positively associated with the daily feeder occupation time of Duroc pigs in our study were also found positively correlated with the appetite of Duroc pigs in a previous study conducted by Yang et al. [46]. One ASV belonging to Lactobacillus genus was found to associate with the daily feeding rate in Duroc pigs at 73 days of age in this study. Lactobacillus strains, commonly used as probiotics promoting overall intestinal health, have been found to influence the host eating behavior through various pathways [47, 48].

The present study also identified 17 ASVs that had negative associations with host feeding behavior traits. At the family level, the majority of these ASVs were classified into Ruminococcaceae, Christensenellaceae, or Family_XIII. Numerous studies have indicated that the intestinal abundance of Christensenellaceae is negatively related to host body mass index and fat mass in human studies [49–51]. Similarly, a significant number of microbes belonging to Ruminococcaceae family colonized in the gut have been associated with the lower weight gain and lean phenotype in humans [52]. In our study, several microbes from the Ruminococcaceae and Christensenellaceae families were negatively associated with daily feeder occupation time or the number of visits to the feeder.

It is possible that the reduced feeding behavior might be linked to the low fatness deposit and weight gain through specific gut taxa, but further studies are needed in this sense. Moreover, both positive and negative associations were identified between microbes from Ruminococcaceae family and feeding behavior measures, including daily feeder occupation time, feed intake per visit to the feeder, and feeding rate across breeds and time points in this study. Similarly, Yang et al. [46] reported one positive and two negative associations between Ruminococcaceae family members and feed intake in pigs.

These findings suggest that Ruminococcaceae family may contain a diverse range of members in the gut, each with distinct functions. Further investigations on the specific individuals belonging to Ruminococcaceae family are needed to clarify this aspect. At the genus level, three ASVs involved in multiple negative associations with the daily feeder occupation time and number of visits to the feeder in several breeds and time points were annotated to Ruminococcaceae_UCG-004, Christensenellaceae_R-7_group, and Family_XIII_AD3011_group. Among these microbes, Christensenellaceae_R-7_group [53], Ruminococcaceae_UCG-004 [54] are known to produce short-chain fatty acids, which are essential metabolites in regulating host energy homeostasis and appetite through gut-brain communication in the gut [55].

Accumulating research has indicated that elevated SCFAs production in the gut could suppress the host appetite [55–57], thus modifying feeding behavior. We identified an ASV belonging to Methanobrevibacter genus in a negative association with the average feeding rate per visit and also in a positive association with the average daily feeder occupation time in Duroc pigs at 123 days in the present study. Interestingly, several studies have shown that people with anorexia nervosa have higher levels of Methanobrevibacter in their gut [58, 59].

The microbes found in this study could serve as candidates for further clarifications on the relationship between the gut microbiota and host feeding behavior. However, differences in the environment [60], experimental design [61], the choice of sequencing platform [62], and 16 S target regions [63] limit the comparisons of results from various microbiome studies. Thus, more studies are still needed to validate the results in different populations with various conditions and further establish the causality between specific microbes and feeding behavior in swine.

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