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Published January 9, 2023 | Published + Supplemental Material
Journal Article Open

Gut microbiota suppress feeding induced by palatable foods

Abstract

Feeding behaviors depend on intrinsic and extrinsic factors including genetics, food palatability, and the environment. The gut microbiota is a major environmental contributor to host physiology and impacts feeding behavior. Here, we explored the hypothesis that gut bacteria influence behavioral responses to palatable foods and reveal that antibiotic depletion (ABX) of the gut microbiota in mice results in overconsumption of several palatable foods with conserved effects on feeding dynamics. Gut microbiota restoration via fecal transplant into ABX mice is sufficient to rescue overconsumption of high-sucrose pellets. Operant conditioning tests found that ABX mice exhibit intensified motivation to pursue high-sucrose rewards. Accordingly, neuronal activity in mesolimbic brain regions, which have been linked with motivation and reward-seeking behavior, was elevated in ABX mice after consumption of high-sucrose pellets. Differential antibiotic treatment and functional microbiota transplants identified specific gut bacterial taxa from the family S24-7 and the genus Lactobacillus whose abundances associate with suppression of high-sucrose pellet consumption. Indeed, colonization of mice with S24-7 and Lactobacillus johnsonii was sufficient to reduce overconsumption of high-sucrose pellets in an antibiotic-induced model of binge eating. These results demonstrate that extrinsic influences from the gut microbiota can suppress the behavioral response toward palatable foods in mice.

Additional Information

The authors thank Dr. Gil Sharon for help with animal behavioral testing and analysis of sequencing data. We are grateful to Drs. Yuki Oka, Viviana Gradinaru, and Scott Kanoski for scientific discussion. We thank Taren Thron, Yvette Garcia-Flores, Mark Adame, and Nikki Cruz for technical and logistical assistance. We thank the Caltech Office of Laboratory Animal Resources (OLAR) and the Institutional Animal Care and Use Committee (IACUC). We acknowledge the Caltech Biological Imaging Facility for microscopy assistance and the Caltech Neurotechnology Laboratory and Caltech TechLab 3D Printing Facility for behavioral equipment fabrication. We thank Dr. Catherine Oikonomou and all members of the Mazmanian Lab for critical evaluation of the manuscript. This work was supported by the National Science Foundation Graduate Research Fellowship under grant no. DGE-1745301 to J.O., the Gates Millennium Scholarship Program to J.O., and funding from the Heritage Medical Research Institute to S.K.M. Author contributions. Conceptualization, J.O. and S.K.M.; investigation, J.O.; formal analysis, J.O. and J.C.B.; writing, J.O.; review, all authors. The authors declare no competing interests.

Attached Files

Published - 1-s2.0-S096098222201750X-main.pdf

Supplemental Material - 1-s2.0-S096098222201750X-mmc1.pdf

Supplemental Material - 1-s2.0-S096098222201750X-mmc2.xlsx

Supplemental Material - 1-s2.0-S096098222201750X-mmc3.xlsx

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Additional details

Created:
August 20, 2023
Modified:
December 22, 2023