Gut microbiota mediate early life stress-induced social dysfunction and anxiety-like behaviors by impairing amino acid transport at the gut

Gut Microbes. 2024 Jan-Dec;16(1):2401939. doi: 10.1080/19490976.2024.2401939. Epub 2024 Sep 11.

Abstract

Early life stress alters gut microbiota and increases the risk of neuropsychiatric disorders, including social deficits and anxiety, in the host. However, the role of gut commensal bacteria in early life stress-induced neurobehavioral abnormalities remains unclear. Using the maternally separated (MS) mice, our research has unveiled a novel aspect of this complex relationship. We discovered that the reduced levels of amino acid transporters in the intestine of MS mice led to low glutamine (Gln) levels in the blood and synaptic dysfunction in the medial prefrontal cortex (mPFC). Abnormally low blood Gln levels limit the brain's availability of Gln, which is required for presynaptic glutamate (Glu) and γ-aminobutyric acid (GABA) replenishment. Furthermore, MS resulted in gut microbiota dysbiosis characterized by a reduction in the relative abundance of Lactobacillus reuteri (L. reuteri). Notably, supplementation with L. reuteri ameliorates neurobehavioral abnormalities in MS mice by increasing intestinal amino acid transport and restoring synaptic transmission in the mPFC. In conclusion, our findings on the role of L. reuteri in regulating intestinal amino acid transport and buffering early life stress-induced behavioral abnormalities provide a novel insight into the microbiota-gut-brain signaling basis for emotional behaviors.

Keywords: Early life stress; gut microbiota; medial prefrontal cortex; neurobehavioral abnormalities; synaptic transmission.

MeSH terms

  • Amino Acid Transport Systems / metabolism
  • Amino Acids / metabolism
  • Animals
  • Anxiety* / metabolism
  • Anxiety* / microbiology
  • Behavior, Animal
  • Brain-Gut Axis / physiology
  • Dysbiosis / microbiology
  • Female
  • Gastrointestinal Microbiome* / physiology
  • Glutamic Acid / metabolism
  • Glutamine / metabolism
  • Male
  • Maternal Deprivation
  • Mice
  • Mice, Inbred C57BL
  • Prefrontal Cortex / metabolism
  • Stress, Psychological* / metabolism
  • Stress, Psychological* / microbiology
  • Synaptic Transmission

Substances

  • Amino Acids
  • Amino Acid Transport Systems
  • Glutamine
  • Glutamic Acid

Grants and funding

This work was supported by grants from the National Natural Science Foundation of China [81703841 to Y. Y.] and Chengdu University of Traditional Chinese Medicine Xinglin Scholars Enhancement Program for Young Scientists [QJRC2021001 to Y. Y.].