Cited by 1,170Gut microbiota and healthProbiotics and Fermented FoodsGABA and Rice Research

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GABA-modulating bacteria of the human gut microbiota

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Strandwitz, Philip, Kim, Ki Hyun, Terekhova, Darya, Liu, Joanne K., Sharma, Anukriti, Levering, Jennifer, McDonald, Daniel, Dietrich, David, Ramadhar, Timothy R., Lekbua, Asama, Mroue, Nader, Liston, Conor, Stewart, Eric J., Dubin, Marc J., Zengler, Karsten, Knight, Rob, Gilbert, Jack A., Clardy, Jon, Lewis, Kim·2018·Nature Microbiology

DOI 10.1038/s41564-018-0307-3PMC PMC6384127

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Abstract

The gut microbiota affects many important host functions, including the immune response and the nervous system1. However, while substantial progress has been made in growing diverse microorganisms of the microbiota2, 23–65% of species residing in the human gut remain uncultured3,4, which is an obstacle for understanding their biological roles. A likely reason for this unculturability is the absence in artificial media of key growth factors that are provided by neighbouring bacteria in situ5,6. In the present study, we used co-culture to isolate KLE1738, which required the presence of Bacteroides fragilis to grow. Bioassay-driven purification of B. fragilis supernatant led to the isolation of the growth factor, which, surprisingly, is the major inhibitory neurotransmitter GABA (γ-aminobutyric acid). GABA was the only tested nutrient that supported the growth of KLE1738, and a genome analysis supported a GABA-dependent metabolism mechanism. Using growth of KLE1738 as an indicator, we isolated a variety of GABA-producing bacteria, and found that Bacteroides ssp. produced large quantities of GABA. Genome-based metabolic modelling of the human gut microbiota revealed multiple genera with the predicted capability to produce or consume GABA. A transcriptome analysis of human stool samples from healthy individuals showed that GABA-producing pathways are actively expressed by Bacteroides, Parabacteroides and Escherichia species. By coupling 16S ribosmal RNA sequencing with functional magentic resonance imaging in patients with major depressive disorder, a disease associated with an altered GABA-mediated response, we found that the relative abundance levels of faecal Bacteroides are negatively correlated with brain signatures associated with depression. A bacterial strain that requires the neurotransmitter GABA for growth was identified and used to isolate GABA-producing bacteria, including Bacteroides spp., from human stool samples; the relative abundance of Bacteroides was negatively correlated with an altered GABA-mediated response in a depression patient cohort.

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Authors: Strandwitz, P., Kim, K. H., Terekhova, D., Liu, J. K., Sharma, A., Levering, J., McDonald, D., Dietrich, D., Ramadhar, T. R., Lekbua, A., Mroue, N., Liston, C., Stewart, E. J., Dubin, M. J., Zengler, K., Knight, R., Gilbert, J. A., Clardy, J., & Lewis, K.
Affiliations: Northeastern University (US)
Harvard University (US)
Weill Cornell Medicine (US)
University of California San Diego (US)
Argonne National Laboratory (US)
Corresponding author: Strandwitz, Philip
Lewis, Kim
ORCID: Strandwitz, Philip
Kim, Ki Hyun
Liu, Joanne K.
Sharma, Anukriti
Levering, Jennifer
McDonald, Daniel
Dietrich, David
Ramadhar, Timothy R.
Lekbua, Asama
Liston, Conor
Dubin, Marc J.
Zengler, Karsten
Knight, Rob
Gilbert, Jack A.
Clardy, Jon
Lewis, Kim
Venue: Nature Microbiology
Publisher: Springer Science and Business Media LLC
Published: 2018-12-10
Volume: 4
Issue: 3
Pages: 396-403
ISSN: 2058-5276 (ISSN-L)
DOI: 10.1038/s41564-018-0307-3
PMC: PMC6384127
OpenAlex: W2902161130
Semantic Scholar: e557d4ef36b36019dcd3ba0973119440d4426bca
Cited by: 1,170
References: 55
Citations by year: 2026: 153 · 2025: 187 · 2024: 225 · 2023: 176 · 2022: 141 · 2021: 131 · 2020: 110 · 2019: 46
FWCI: 26.77
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springernature.com/gp/researchers/text-and-data-mining (tdm)
www.springernature.com/gp/researchers/text-and-data-mining (vor)
Locations: Nature Microbiology (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
eScholarship (California Digital Library) (submittedVersion)
Funders: National Institutes of Health
Faculty of Arts and Sciences
National Human Genome Research Institute (R01HG005824)
National Institute of General Medical Sciences (F32GM108415)
National Institute of Allergy and Infectious Diseases (R01AI122286)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
Life Sciences › Agricultural and Biological Sciences › Plant Science › GABA and Rice Research
Keywords: GABA, gut microbiota, Bacteroides, GABA-producing bacteria, bacterial growth factors, co-culture, Bacteroides fragilis, Parabacteroides, Escherichia, major depressive disorder, functional MRI, neurotransmitter metabolism, uncultured bacteria
MeSH terms: Gastrointestinal Microbiome, Whole Genome Sequencing, Adult, Aged, Bacteria, Bacteroides, Brain, Depression, Depressive Disorder, Major, Major Depressive Disorder, Feces, Female, gamma-Aminobutyric Acid, Humans, Magnetic Resonance Imaging, Male, Middle Aged, Cohort Studies, Gene Expression Profiling, Gastrointestinal Tract, Young Adult

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