Ulcerative colitis (UC) is associated with brain neurotransmitter
disorders and intestinal dysbiosis. Bacillus amyloliquefaciens fmb50 produces the lipopeptide surfactin, which has a wide range
of biological activities. However, the effects of surfactin on DSS-induced
colitis have not been reported. In the present study, oral surfactin
significantly ameliorated colitis in a mouse model and reduced depression-like
behavior, such as slowed walking speed, shortened movement distance
in the open field test, and weakened exploration ability in the light–dark
shuttle test. Surfactin noticeably improved gut microbial dysbiosis,
intestinal barrier dysfunction in the colon, and blood–brain
barrier dysfunction in the brain. Furthermore, the colon levels of
occludin were upregulated by 68.51%, and the brain levels of occludin
and ZO-1 were upregulated by 77.81% and 36.42%, respectively. Surfactin
supplementation also inhibited inflammatory responses by inactivating
the tumor necrosis factor-α (TNF-α), nuclear factor kappa-B
(NF-κB), and NLRP3 signaling pathways in the colon and brain.
Thus, we believe that surfactin improved the behavioral disorders
by upregulating the levels of 5-hydroxytryptamine (5-HT), 5-hydroxyindoleacetic
acid (5-HIAA), norepinephrine (NE), and brain-derived neurotrophic
factor (BDNF), suppressing the inflammatory responses, and improving
the blood–brain barrier dysfunction. Surfactin also reduced
the abundances of gut microbes that are related to colitis, especially
targeting facultative anaerobes of the phylum Proteobacteria, and
it increased the abundance of beneficial bacteria such as Lactobacillus and unidentified Prevotella. Combined with its nontoxic nature observed in this long-term study
in mice, oral surfactin might be a promising intervention strategy
for preventing colitis by acting on the microbiota-gut–brain
axis.