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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“85”
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Background
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BackgroundInfluential
Gut microbiota supports male reproduction via nutrition, immunity, and signaling
Cai, H., Cao, X., Qin, D., Liu, Y., Liu, Y., Hua, J., & Peng, S. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.977574 · Cited by 75
“GABA Promotes sperm capacitation and acrosomal reaction; reduces the excessive activation of sperm; increases libido and sexual behavior Bacteroides, Parabacter and Escherichia coli (Strandwitz et al., 2019)”
Background
A review of the impact of herbicides and insecticides on the microbial communities
Aravind, J., Kamaraj, M., Thayanithi, S., & Palanisamy, S. B. (2023) · Environmental Research · doi:10.1016/j.envres.2023.118020 · Cited by 68
The diet-microbiome tango: how nutrients lead the gut brain axis
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“Furthermore, the gut microbiome relies on the host diet content to produce neuromodulators such as g -aminobutyric acid (GABA) [27 ], provides nutrients to the host, and modiﬁes the availability of speciﬁc nutrients derived from the diet, thereby deeply shaping the nutritional environment of the…”
Background
Our Mental Health Is Determined by an Intrinsic Interplay between the Central Nervous System, Enteric Nerves, and Gut Microbiota
Dicks, L. M. T. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms25010038 · Cited by 74
“D-Glu is then decarboxylated by Glu decarboxylase (GAD; EC 4.1.1.15) to GABA [72,73].”
BackgroundInfluential
GABAergic implications in anxiety and related disorders
Arora, I., Mal, P., Arora, P., Paul, A., & Kumar, M. (2024) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2024.150218 · Cited by 74
Microbiota-brain axis: Exploring the role of gut microbiota in psychiatric disorders - A comprehensive review
Singh, J., Vanlallawmzuali, Singh, A. K., Biswal, S., Zomuansangi, R., Lalbiaktluangi, C., Singh, B. P., Singh, P. K., Vellingiri, B., Iyer, M., et al. (2024) · Asian Journal of Psychiatry · doi:10.1016/j.ajp.2024.104068 · Cited by 71
The Role of the Gut-Brain Axis in Attention-Deficit/Hyperactivity Disorder
Dam, S. A., Mostert, J. C., Szopinska-Tokov, J., Bloemendaal, M., Amato, M. P., & Vásquez, A. A. (2019) · Gastroenterology Clinics of North America · doi:10.1016/j.gtc.2019.05.001 · Cited by 66
Alterations of the Composition and Neurometabolic Profile of Human Gut Microbiota in Major Depressive Disorder
Kovtun, A. S., Averina, O. V., Angelova, I. Y., Yunes, R. А., Zorkina, Y., Morozova, A. Y., Pavlichenko, A. V., Syunyakov, T., Karpenko, O., Kostyuk, G. P., et al. (2022) · Biomedicines · doi:10.3390/biomedicines10092162 · Cited by 67
“GLU and its metabolite GABA are known as key excitatory or inhibitory neurotransmitters in the neurovascular system, and dysfunctions in their signaling pathways are closely related to depression [95,96].”
Background
A systematic review exploring the association between the human gut microbiota and brain connectivity in health and disease
Mulder, D., Aarts, E., Vásquez, A. A., & Bloemendaal, M. (2023) · Molecular Psychiatry · doi:10.1038/s41380-023-02146-4 · Cited by 70
“…in association with the gut microbiota in seven out of nine studies: six out of six studies reported associations between ICA-based DMN-connectivity and the gut microbiota [27 – 31, 36 – 38, 42], and associations with the precuneus were reported in three out of six studies [27 – 29, 38, 44].”
BackgroundResult
Biosensing in Smart Engineered Probiotics
Rottinghaus, A. G., Amrofell, M. B., & Moon, T. S. (2019) · Biotechnology Journal · doi:10.1002/biot.201900319 · Cited by 63
Parabacteroides distasonis induces depressive-like behavior in a mouse model of Crohn’s disease
Gomez-Nguyen, A., Basson, A. R., Dark, L. M., Hsu, K., Ösme, A., Menghini, P., Pizarro, T. T., & Cominelli, F. (2021) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2021.08.218 · Cited by 63
Microbiota-gut-brain axis in autism spectrum disorder
Yu, Y., & Zhao, F. (2021) · Journal of genetics and genomics/Journal of Genetics and Genomics · doi:10.1016/j.jgg.2021.07.001 · Cited by 64
Gut microbiota and neuropsychiatric disorders: Implications for neuroendocrine-immune regulation
Ge, T., Yao, X., Zhao, H., Yang, W., Zou, X., Peng, F., Li, B., & Cui, R. (2021) · Pharmacological Research · doi:10.1016/j.phrs.2021.105909 · Cited by 62
SCFAs Supplementation Rescues Anxiety- and Depression-like Phenotypes Generated by Fecal Engraftment of Treatment-Resistant Depression Rats
Palepu, M. S. K., Gajula, S. N. R., Malleshwari, K., Sonti, R., & Dandekar, M. P. (2024) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.3c00727 · Cited by 65
Gut Microbiota Regulate Astrocytic Functions in the Brain: Possible Therapeutic Consequences
Zhao, Y.-F., Wei, D., & Tang, Y. (2021) · Current Neuropharmacology · doi:10.2174/1570159x19666210215123239 · Cited by 60
“It was reported that neuroinflammatory genes, notably Tnf encoding tumor necrosis factor-α (TNF-α), were upregulated in the opioid withdrawal condition in highly active astrocytes of the amygdala, and in parallel, a decreased Firmicutes to Bacteroides ratio indicated gut dysbiosis [43].”
Background
Dietary palmitoleic acid reprograms gut microbiota and improves biological therapy against colitis
Chen, Y., Mai, Q., Chen, Z., Lin, T., Cai, Y., Han, J., Wang, Y., Zhang, M., Tan, S. K., Wu, Z., et al. (2023) · Gut Microbes · doi:10.1080/19490976.2023.2211501 · Cited by 64
Mechanisms for the biological activity of Gastrodia elata Blume and its constituents: A comprehensive review on sedative-hypnotic, and antidepressant properties
Zhou, H., Lu, S.-Z., Yu, Z.-S., Zhang, J., & Mei, Z. (2023) · Phytomedicine · doi:10.1016/j.phymed.2023.155251 · Cited by 61
Gut microbiome: An intermediary to neurotoxicity
Dempsey, J. L., Little, M., & Cui, J. Y. (2019) · NeuroToxicology · doi:10.1016/j.neuro.2019.08.005 · Cited by 63
“Co-cultures of multiple microbial species may be the solution to this problem, and this method has been shown to be successful in characterizing GABA-modulating bacteria in the human gut (Strandwitz et al., 2019).”
Method
A comparison of the gut microbiota among adult patients with drug-responsive and drug-resistant epilepsy: an exploratory study
Lee, H., Lee, S., Lee, D.-H., & Kim, D. W. (2021) · Epilepsy Research · doi:10.1016/j.eplepsyres.2021.106601 · Cited by 57
Gut microbiome predicts cognitive function and depressive symptoms in late life
Kolobaric, A., Andreescu, C., Jašarević, E., Hong, C. H., Roh, H., Cheong, J. Y., Kim, Y., Shin, T. S., Kang, C. S., Kwon, C. O., et al. (2024) · Molecular Psychiatry · doi:10.1038/s41380-024-02551-3 · Cited by 63
“Interest-ingly, higher baseline Bacteroidota associated with lower baseline cognitive function, while lower baseline Bacteroidota also associated with future depression increase, emphasizing Bacter-oidota is a large phylum with a variety of species that differently impact host health.”
Background
From bugs to brain: unravelling the GABA signalling networks in the brain–gut–microbiome axis
Belelli, D., Lambert, J. J., Wan, M. L. Y., Monteiro, A. R., Nutt, D., & Swinny, J. D. (2024) · Brain · doi:10.1093/brain/awae413 · Cited by 69
“156 Indeed, inulin-degrading species are widely distributed across Bacteroides and Eubacterium , 404 and these strains may play an indirect role in a healthy gut (see later).”
Influential
Sexual Dimorphism of Gut Microbiota Dictates Therapeutics Efficacy of Radiation Injuries
Cui, M., Xiao, H., Li, Y., Zhang, S., Dong, J., Wang, B., Zhu, C., Jiang, M., Zhu, T., He, J., et al. (2019) · Advanced Science · doi:10.1002/advs.201901048 · Cited by 59
Tauroursodeoxycholic acid (TUDCA) is neuroprotective in a chronic mouse model of Parkinson’s disease
Cuevas, E., Burks, S., Raymick, J., Robinson, B., Gómez-Crisóstomo, N. P., Escudero-Lourdes, C., Lopez, A. G. G., Chigurupati, S., Hanig, J., Ferguson, S. A., et al. (2022) · Nutritional Neuroscience · doi:10.1080/1028415x.2020.1859729 · Cited by 57
“suggested that bacteria have the capacity to generate or breakdown GABA and have been implicated in host health, including behavior [62].”
Background
Gut Microbial Metabolites in Parkinson’s Disease: Implications of Mitochondrial Dysfunction in the Pathogenesis and Treatment
Liang, Y., Cui, L., Gao, J., Zhu, M., Zhang, Y., & Zhang, H. (2021) · Molecular Neurobiology · doi:10.1007/s12035-021-02375-0 · Cited by 59
Effect of Anesthesia/Surgery on Gut Microbiota and Fecal Metabolites and Their Relationship With Cognitive Dysfunction
Lian, X., Zhu, Q., Li, S., & Cheng, Y. (2021) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2021.655695 · Cited by 57
“In agreement with the above findings, the GABA precursors pyroglutamic acid and glutamate acid were enriched after anesthesia/surgery (Strandwitz et al., 2019), implying that elevated levels of GABA precursors might be induced by enriched Escherichia–Shigella.”
Result
Are We What We Eat? Impact of Diet on the Gut–Brain Axis in Parkinson’s Disease
Alfonsetti, M., Castelli, V., & d’Angelo, M. (2022) · Nutrients · doi:10.3390/nu14020380 · Cited by 61
“For example, the lytic Lactococcus phages are more numerous in PD patients than in healthy people, which is related to a sharp decrease in Lactococcus bacteria [94] since these bacteria are able to release the neurotransmitter dopamine [95] and regulate gut permeability [96].”
Background
Role of Short Chain Fatty Acids in Epilepsy and Potential Benefits of Probiotics and Prebiotics: Targeting “Health” of Epileptic Patients
Kim, S., Park, S., Choi, T. G., & Kim, S. S. (2022) · Nutrients · doi:10.3390/nu14142982 · Cited by 62
The gut microbiota to the brain axis in the metabolic control
Grasset, E., & Burcelin, R. (2019) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-019-09511-1 · Cited by 57
The potential of human milk oligosaccharides to impact the microbiota-gut-brain axis through modulation of the gut microbiota
Al-Khafaji, A. H., Jepsen, S. D., Christensen, K. R., & Vigsnæs, L. K. (2020) · Journal of Functional Foods · doi:10.1016/j.jff.2020.104176 · Cited by 62
Targeting the microbiome-gut-brain axis for improving cognition in schizophrenia and major mood disorders: A narrative review
Bioque, M., González-Rodríguez, A., García‐Rizo, C., Cobo, J., Monreal, J. A., Usall, J., Soria, V., & Labad, J. (2020) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2020.110130 · Cited by 58
Emerging trends and focus of human gastrointestinal microbiome research from 2010–2021: a visualized study
Yuan, X., Chang, C., Chen, X., & Li, K. (2021) · Journal of Translational Medicine · doi:10.1186/s12967-021-03009-8 · Cited by 60
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Background
The Gut Microbiome–Brain Crosstalk in Neurodegenerative Diseases
Ghezzi, L., Cantoni, C., Rotondo, E., & Galimberti, D. (2022) · Biomedicines · doi:10.3390/biomedicines10071486 · Cited by 61
“GABA-producing pathways are expressed by Bacteroides, Parabacteroides, and Escherichia species [56].”
Background
Exploring the Potential of Lactobacillus helveticus R0052 and Bifidobacterium longum R0175 as Promising Psychobiotics Using SHIME
de Oliveira, F. L., Salgaço, M. K., de Oliveira, M. T., Mesa, V., Sartoratto, A., da Silva, A. M. P., Ramos, W. S., & Sivieri, K. (2023) · Nutrients · doi:10.3390/nu15061521 · Cited by 61
“0), glutamate decarboxylation is induced and produces GABA, which is then exported from the cell in a protonated form, alkalizing the cytoplasm [87].”
Background
Microbiome-targeted interventions for the control of oral–gut dysbiosis and chronic systemic inflammation
Pacheco‐Yanes, J., Reynolds, E. C., Li, J., & Mariño, E. (2023) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2023.08.006 · Cited by 59
Differences in the Concentration of the Fecal Neurotransmitters GABA and Glutamate Are Associated with Microbial Composition among Healthy Human Subjects
Altaib, H., Nakamura, K., Abe, M., Badr, Y., Yanase, E., Nomura, I., & Suzuki, T. (2021) · Microorganisms · doi:10.3390/microorganisms9020378 · Cited by 56
“It has been reported that mental disorders, such as depression, are negatively correlated with the abundance of GABA-producing Bacteroides [14].”
Background
Revisiting the Bacterial Phylum Composition in Metabolic Diseases Focused on Host Energy Metabolism
Lee, Y., & Lee, H. (2020) · Diabetes & Metabolism Journal · doi:10.4093/dmj.2019.0220 · Cited by 56
“Additionally, some strains of human gut microbiota can produce a neuroactive metabolite like γ-aminobutyric acid (GABA), the major inhibitory neurotransmitter, which is involved in hypothalamic appetite stimulation [46,51].”
Background
Chronic Effects of Dietary Pesticides on the Gut Microbiome and Neurodevelopment
Gama, J. S., Neves, B. C., & Pereira, A. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.931440 · Cited by 58
Role of gut microbiota in depression: Understanding molecular pathways, recent research, and future direction
Rathour, D., Shah, S., Khan, S., Singh, P. K., Srivastava, S., Singh, S. B., & Khatri, D. K. (2022) · Behavioural Brain Research · doi:10.1016/j.bbr.2022.114081 · Cited by 58
Targeting the blood–brain barrier to delay aging-accompanied neurological diseases by modulating gut microbiota, circadian rhythms, and their interplays
Wang, Y., Du, W., Hu, X., Yu, X., Guo, C., Jin, X., & Wang, W. (2023) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2023.08.009 · Cited by 58
“Interestingly, gut microbiota-derived GABA shows neuroprotective effects in Clostridium elegans , highlighting the role of bacterially-produced GABA in keeping brain homeostasis 205 .”
Background
Exploring the complex relationship between psychosocial stress and the gut microbiome: implications for inflammation and immune modulation
Marwaha, K., Cain, R., Asmis, K., Czaplinski, K., Holland, N. A., Mayer, D. C. G., & Chacon, J. A. (2025) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00652.2024 · Cited by 65
Molecules from the Microbiome
Shine, E. E., & Crawford, J. M. (2021) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-080320-115307 · Cited by 55
Strategies for culturing active/dormant marine microbes
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Effects of microbial-derived biotics (meta/pharma/post-biotics) on the modulation of gut microbiome and metabolome; general aspects and emerging trends
Sadeghi, A., Ebrahimi, M. T., Kharazmi, M. S., & Jafari, S. M. (2023) · Food Chemistry · doi:10.1016/j.foodchem.2023.135478 · Cited by 58
The Involvement of Neuroinflammation in the Onset and Progression of Parkinson’s Disease
Jurcău, A., Andronie-Cioară, F. L., Nistor-Cseppento, C. D., Pașcalău, N., Rus, M., Vasca, E., & Jurcău, M. C. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241914582 · Cited by 58
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Physical Exercise as Disease-Modifying Alternative against Alzheimer’s Disease: A Gut–Muscle–Brain Partnership
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“In fact, some bacterial genera such as Escherichia coli, Bacteroides, Eubacterium, and Bifidobacterium are involved in the production of neurotransmitters such as acetylcholine, GABA, and glutamate, and alterations in these were found in AD patients [105,106].”
Background
Alleviating effect of vagus nerve cutting in Salmonella-induced gut infections and anxiety-like behavior via enhancing microbiota-derived GABA
Zou, Q., Han, S., Liang, J., Yan, G., Wang, Q., Wang, Y., Zhang, Z., Hu, J., Li, J., Tian, Y., et al. (2024) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2024.04.034 · Cited by 54

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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