Postnatal colonization with human "infant-type" Bifidobacterium species alters behavior of adult gnotobiotic mice
Open accessAbstract
Accumulating studies have defined a role for the intestinal microbiota in modulation of host behavior. Research using gnotobiotic mice emphasizes that early microbial colonization with a complex microbiota (conventionalization) can rescue some of the behavioral abnormalities observed in mice that grow to adulthood completely devoid of bacteria (germ-free mice). However, the human infant and adult microbiomes vary greatly, and effects of the neonatal microbiome on neurodevelopment are currently not well understood. Microbe-mediated modulation of neural circuit patterning in the brain during neurodevelopment may have significant long-term implications that we are only beginning to appreciate. Modulation of the host central nervous system by the early-life microbiota is predicted to have pervasive and lasting effects on brain function and behavior. We sought to replicate this early microbe-host interaction by colonizing gnotobiotic mice at the neonatal stage with a simplified model of the human infant gut microbiota. This model consortium consisted of four "infant-type" Bifidobacterium species known to be commensal members of the human infant microbiota present in high abundance during postnatal development. Germ-free mice and mice neonatally-colonized with a complex, conventional murine microbiota were used for comparison. Motor and non-motor behaviors of the mice were tested at 6-7 weeks of age, and colonization patterns were characterized by 16S ribosomal RNA gene sequencing. Adult germ-free mice were observed to have abnormal memory, sociability, anxiety-like behaviors, and motor performance. Conventionalization at the neonatal stage rescued these behavioral abnormalities, and mice colonized with Bifidobacterium spp. also exhibited important behavioral differences relative to the germ-free controls. The ability of Bifidobacterium spp. to improve the recognition memory of both male and female germ-free mice was a prominent finding. Together, these data demonstrate that the early-life gut microbiome, and human "infant-type" Bifidobacterium species, affect adult behavior in a strongly sex-dependent manner, and can selectively recapitulate the results observed when mice are colonized with a complex microbiota.
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A mixture of 'infant type' Bifidobacterium strains improved cognitive deficits in GF mice.
“More recently, a mixture of 'infant type' Bifidobacterium strains had the same beneficial effects improving the cognitive deficits in GF mice (Luk et al., 2018), suggesting the importance of early-life microbiota in adult cognitive behavior.”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Luk et al., 2018
GF mice exhibit an impaired ability to remember a familiar object when presented with a novel object.
“It has been shown that GF mice exhibit an impaired ability to remember a familiar object when presented with a novel object (Gareau et al., 2011;Luk et al., 2018), as well as impaired working memory in remembering a familiar environment in the spontaneous alternation task (Gareau et al., 2011).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Luk et al., 2018
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- Authors
- Luk, B., Veeraragavan, S., Engevik, M., Balderas, M., Major, A., Runge, J., Luna, R. A., & Versalovic, J.
- Affiliations
- Baylor College of Medicine (US)
- Texas Children's Hospital (US)
- Corresponding author
- Versalovic, James
- ORCID
- Venue
- PLOS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2018-05-15
- Volume
- 13
- Issue
- 5
- Pages
- e0196510
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC5953436
- OpenAlex
- W2803786491
- Cited by
- 90
- References
- 71
- Citations by year
- 2026: 7 · 2025: 9 · 2024: 10 · 2023: 12 · 2022: 12 · 2021: 18 · 2020: 9 · 2019: 10 · 2018: 3
- FWCI
- 3.56
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- PLoS ONE (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Funders
- National Cancer Institute (U01 CA170930)
- National Institutes of Health (P30 DK56338)
- Biogaia AB
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (U54HD083092)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Keywords
- infant gut microbiota, Bifidobacterium, neonatal colonization, gnotobiotic mice, germ-free mice, recognition memory, anxiety-like behavior, sociability, motor behavior, sex differences, brain development, early-life microbial colonization
- MeSH terms
- Gastrointestinal Microbiome, Animals, Animals, Newborn, Anxiety, Behavior, Animal, Bifidobacterium, Female, Germ-Free Life, Humans, Infant, Male, Memory, Motor Skills, Social Behavior, Specific Pathogen-Free Organisms, Models, Animal, Mice
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