gamma-Aminobutyric acid uptake by a bacterial system with neurotransmitter binding characteristics.
Open accessAbstract
gamma-Aminobutyric acid (GABA), an amino acid, has been found in every class of living organisms. In higher organisms, GABA is a neurotransmitter and binds with high affinity and specificity to GABA receptors on neurons in a sodium-independent reaction that is saturable. The role of GABA in organisms lacking nervous tissue is not known. This report describes, in a strain of Pseudomonas fluorescens, a GABA uptake system with binding characteristics like those of the GABA (type A) brain receptor. The binding was saturable and specific for GABA, was sodium-independent, was of high affinity (Km = 65 nM), and was inhibited competitively by muscimol, a potent GABA analogue. The bacterial GABA system included a homogeneous binding site, and no cooperative interaction was found between sites. To our knowledge, such a system for GABA, or other neurotransmitters, in a bacterium has not been reported.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Bacteria express receptors capable of sensing extracellular GABA.
“bacteria express receptors capable of sensing extracellular, GABA (Guthrie and Nicholson-Guthrie, 1989).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Guthrie and Nicholson-Guthrie, 1989
Cites
PROTEIN MEASUREMENT WITH THE FOLIN PHENOL REAGENT
Lowry, O. H., Rosebrough, N., Farr, A. L., & Randall, R. (1951) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)52451-6 · Cited by 315,771 · see citing works
Deoxyribonucleic acid replication in meiosis of Chlamydomonas reinhardi
Sueoka, N., Chiang, K. S., & Kates, J. R. (1967) · Journal of Molecular Biology · doi:10.1016/0022-2836(67)90278-1 · Cited by 351 · see citing works
Krogsgaard‐Larsen, P., & Johnston, G. A. R. (1975) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1975.tb04410.x · Cited by 328 · see citing works
The Evolutionary Origins of Hormones, Neurotransmitters, and Other Extracellular Chemical Messengers
Bleich, H. L., Moore, M. J., Roth, J., LeRoith, D., Shiloach, J., Rosenzweig, J. L., Lesniak, M. A., & Havránková, J. (1982) · New England Journal of Medicine · doi:10.1056/nejm198203043060907 · Cited by 229 · see citing works
Biochemical and Electrophysiological Characteristics of Mammalian Gaba Receptors
Enna, S. J., & Gallagher, J. P. (1983) · International review of neurobiology · doi:10.1016/s0074-7742(08)60222-6 · Cited by 137 · see citing works
Biochemical dissection of the γ-aminobutyrate synapse
Turner, A. J., & Whittle, S. R. (1983) · Biochemical Journal · doi:10.1042/bj2090029 · Cited by 118 · see citing works
Eldefrawi, A. T., & Eldefrawi, M. E. (1987) · The FASEB Journal · doi:10.1096/fasebj.1.4.2443413 · Cited by 108 · see citing works
Bacterial Chemotaxis in Relation to Neurobiology
Koshland, D. E. (1980) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.03.030180.000355 · Cited by 97 · see citing works
Horng, J. S., & Wong, D. T. (1979) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1979.tb11075.x · Cited by 53 · see citing works
Muscimol and the uptake of ?-aminobutyric acid by rat brain slices
Johnston, G. A. R. (1971) · Psychopharmacology · doi:10.1007/bf00401785 · Cited by 50 · see citing works
Amino Acid Transport in Pseudomonas aeruginosa
Kay, W. W., & Gronlund, A. F. (1969) · Journal of Bacteriology · doi:10.1128/jb.97.1.273-281.1969 · Cited by 49 · see citing works
Gamma-aminobutyric Acid (GABA) Production by Eight Common Bacterial Pathogens
Minuk, G. Y. (1986) · Scandinavian Journal of Infectious Diseases · doi:10.3109/00365548609032366 · Cited by 40 · see citing works
Specificity and Regulation of γ-Aminobutyrate Transport in Escherichia coli
Kahane, S., Levitz, R., & Halpern, Y. S. (1978) · Journal of Bacteriology · doi:10.1128/jb.135.2.295-299.1978 · Cited by 24 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Cryan, J. F., O'Riordan, K. J., Cowan, C. S. M., Sandhu, K. V., Bastiaanssen, T. F. S., Boehme, M., Codagnone, M. G., Cussotto, S., Fulling, C., Golubeva, A. V., et al. (2019) · Physiological Reviews · doi:10.1152/physrev.00018.2018 · Cited by 5,286 · see citing works
The gut-brain axis: interactions between enteric microbiota, central and enteric nervous systems.
(2015) · PubMed Central · Cited by 2,540 · see citing works
Forsythe, P., Sudo, N., Dinan, T., Taylor, V. H., & Bienenstock, J. (2010) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2009.05.058 · Cited by 429 · see citing works
The Neuro-endocrinological Role of Microbial Glutamate and GABA Signaling
Mazzoli, R., & Pessione, E. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.01934 · Cited by 383 · see citing works
A genetically encoded fluorescent sensor for in vivo imaging of GABA
Marvin, J. S., Shimoda, Y., Magloire, V., Leite, M., Kawashima, T., Jensen, T. P., Kolb, I., Knott, E. L., Novák, O., Podgorski, K., et al. (2019) · Nature Methods · doi:10.1038/s41592-019-0471-2 · Cited by 350 · see citing works
Why does the microbiome affect behaviour?
Johnson, K. V.-A., & Foster, K. R. (2018) · Nature Reviews Microbiology · doi:10.1038/s41579-018-0014-3 · Cited by 333 · see citing works
Microbial endocrinology and infectious disease in the 21st century
Lyte, M. (2004) · Trends in Microbiology · doi:10.1016/j.tim.2003.11.004 · Cited by 268 · see citing works
The intestinal microbiome, probiotics and prebiotics in neurogastroenterology
Saulnier, D. M., Ringel, Y., Heyman, M. B., Foster, J. A., Bercik, P., Shulman, R. J., Versalovic, J., Verdu, E. F., Dinan, T. G., Hecht, G., et al. (2013) · Gut Microbes · doi:10.4161/gmic.22973 · Cited by 248 · see citing works
Lyte, M. (2014) · Gut Microbes · doi:10.4161/gmic.28682 · Cited by 225 · see citing works
Mind-altering with the gut: Modulation of the gut-brain axis with probiotics
Kim, N., Yun, M., Oh, Y. J., & Choi, H.-J. (2018) · Journal of Microbiology · doi:10.1007/s12275-018-8032-4 · Cited by 210 · see citing works
Role of the Gut Microbiome in Autism Spectrum Disorders
Pulikkan, J., Mazumder, A., & Grace, T. (2019) · Advances in Experimental Medicine and Biology · doi:10.1007/978-3-030-05542-4_13 · Cited by 142 · see citing works
Evtushenko, L. I., & Takeuchi, M. (2006) · Springer eBooks · doi:10.1007/0-387-30743-5_43 · Cited by 141 · see citing works
Distler, M. G., & Palmer, A. A. (2012) · Frontiers in Genetics · doi:10.3389/fgene.2012.00250 · Cited by 112 · see citing works
Role of Gut Microbiota in Neurological Disorders and Its Therapeutic Significance
Tiwari, P., Dwivedi, R., Bansal, M., Tripathi, M., & Dada, R. (2023) · Journal of Clinical Medicine · doi:10.3390/jcm12041650 · Cited by 106 · see citing works
Epigenetics in depression and gut-brain axis: A molecular crosstalk
Begum, N., Mandhare, A., Tryphena, K. P., Srivastava, S., Shaikh, M. F., Singh, S. B., & Khatri, D. K. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.1048333 · Cited by 99 · see citing works
The microbiota-gut-brain axis: Focus on the fundamental communication pathways
Bistoletti, M., Bosi, A., Banfi, D., Giaroni, C., & Baj, A. (2020) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2020.08.012 · Cited by 88 · see citing works
Gram-Negative Bacterial Sensors for Eukaryotic Signal Molecules
Lesouhaitier, O., Véron, W., Chapalain, A., Madi, A., Blier, A.-S., Dagorn, A., Connil, N., Chevalier, S., Orange, N., & Feuilloley, M. G. J. (2009) · Sensors · doi:10.3390/s90906967 · Cited by 71 · see citing works
The microbiota-gut-brain axis: An emerging role for the epigenome
Louwies, T., Johnson, A. C., Orock, A. M., Yuan, T., & Meerveld, B. G. (2019) · Experimental Biology and Medicine · doi:10.1177/1535370219891690 · Cited by 66 · see citing works
Molecular assemblies of functionalized polydiacetylenes
Spevak, W. R., Nagy, J. O., & Charych, D. H. (1995) · Advanced Materials · doi:10.1002/adma.19950070120 · Cited by 64 · see citing works
Dagorn, A., Chapalain, A., Mijouin, L., Hillion, M., Poc, C. D., Chevalier, S., Taupin, L., Orange, N., & Feuilloley, M. G. J. (2013) · International Journal of Molecular Sciences · doi:10.3390/ijms140612186 · Cited by 61 · see citing works
as a potential pathogen: adherence to nerve cells
Picot, L., Mezghani-Abdelmoula, S., Mérieau, A., Leroux, P., Cazin, L., Orange, N., & Feuilloley, M. G. J. (2001) · Microbes and Infection · doi:10.1016/s1286-4579(01)01462-9 · Cited by 57 · see citing works
The microbiome and gut endocannabinoid system in the regulation of stress responses and metabolism
Srivastava, R. K., Lutz, B., & Ruiz de Azua, I. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2022.867267 · Cited by 56 · see citing works
Potential Roles for Gamma-Aminobutyric Acid Signaling in Bacterial Communities
Quillin, S. J., Tran, P., & Prindle, A. B. (2021) · Bioelectricity · doi:10.1089/bioe.2021.0012 · Cited by 54 · see citing works
Role of Microbiome in Regulating the HPA Axis and Its Relevance to Allergy
Sudo, N. (2012) · Chemical Immunology and Allergy · doi:10.1159/000336510 · Cited by 54 · see citing works
Gamma-aminobutyric acid acts as a specific virulence regulator in Pseudomonas aeruginosa
Dagorn, A., Hillion, M., Chapalain, A., Lesouhaitier, O., Duclairoir Poc, C., Vieillard, J., Chevalier, S., Taupin, L., Le Derf, F., & Feuilloley, M. G. J. (2013) · Microbiology · doi:10.1099/mic.0.061267-0 · Cited by 51 · see citing works
Concas, A., Pierobon, P., Mostallino, M. C., Marino, G., Minei, R., & Biggio, G. (1998) · Neuroscience · doi:10.1016/s0306-4522(97)00515-0 · Cited by 50 · see citing works
The amino acid sequence of glutamate decarboxylase from Escherichia coli
Maras, B., Sweeney, G. E., Barra, D., Bossa, F., & John, R. A. (1992) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1992.tb16609.x · Cited by 50 · see citing works
Yan, R., Ho, C., & Zhang, X. (2020) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.202000187 · Cited by 49 · see citing works
Urine GABA levels in ovarian cancer patients:
Nicholson-Guthrie, C. S., Guthrie, G. D., Sutton, G. P., & Baenziger, J. C. (2001) · Cancer Letters · doi:10.1016/s0304-3835(00)00620-0 · Cited by 40 · see citing works
Self-citationMicrobial Endocrinology: An Ongoing Personal Journey
Lyte, M. (2016) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-20215-0_1 · Cited by 35 · see citing works
Cytotoxic effects of the lipopolysaccharide from Pseudomonas fluorescens on neurons and glial cells
Picot, L., Chevalier, S., Mezghani-Abdelmoula, S., Mérieau, A., Lesouhaitier, O., Leroux, P., Cazin, L., Orange, N., & Feuilloley, M. G. J. (2003) · Microbial Pathogenesis · doi:10.1016/s0882-4010(03)00092-5 · Cited by 31 · see citing works
Neuroimmune aspects of food intake
Bienenstock, J., Forsythe, P., Karimi, K., & Kunze, W. (2009) · International Dairy Journal · doi:10.1016/j.idairyj.2009.12.002 · Cited by 30 · see citing works
Advances in Engineering and Application of Optogenetic Indicators for Neuroscience
Piatkevich, K. D., Murdock, M. H., & Subach, F. V. (2019) · Applied Sciences · doi:10.3390/app9030562 · Cited by 30 · see citing works
A Bacterial High-Affinity GABA Binding Protein: Isolation and Characterization
Guthrie, G. D., Nicholson-Guthrie, C. S., & Leary, H. L. (2000) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1999.1960 · Cited by 26 · see citing works
Self-citationMicrobial Endocrinology: A Personal Journey
Lyte, M. (2010) · Springer eBooks · doi:10.1007/978-1-4419-5576-0_1 · Cited by 18 · see citing works
Raj, K., Singh, S., Chib, S., & Mallan, S. (2022) · Current Pharmaceutical Design · doi:10.2174/1381612828666221003112300 · Cited by 16 · see citing works
You, X., Yang, W., Li, X., Li, X., Huang, Y., & Huang, C. (2025) · Journal of Endocrinological Investigation · doi:10.1007/s40618-025-02615-3 · Cited by 15 · see citing works
Zhang, Y., Zheng, Y., Qin, L., Wang, S., Buchko, G. W., & Garavito, R. M. (2014) · Biochimie · doi:10.1016/j.biochi.2014.05.002 · Cited by 15 · see citing works
Probiotic and prebiotic interventions in eating disorders: A narrative review
Baenas, I., Camacho‐Barcia, L., Miranda‐Olivos, R., Solé‐Morata, N., Misiolek, A., Jiménez‐Múrcia, S., & Fernández‐Aranda, F. (2024) · European Eating Disorders Review · doi:10.1002/erv.3069 · Cited by 14 · see citing works
Song, C., Gao, X., Song, W., Zeng, D., Shan, S., Yin, Y., Li, Y., Baranenko, D., & Lu, W. (2020) · RSC Advances · doi:10.1039/d0ra01017k · Cited by 14 · see citing works
The role of the gut microbiome in neuroinflammation and chemotherapy-induced peripheral neuropathy
Shatunova, S., Aktar, R., Peiris, M., Lee, J. Y. P., Vetter, I., & Starobova, H. (2024) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2024.176818 · Cited by 14 · see citing works
Mezghani-Abdelmoula, S., Chevalier, S., Lesouhaitier, O., Orange, N., Feuilloley, M. G. J., & Cazin, L. (2003) · Brain Research · doi:10.1016/s0006-8993(03)03055-5 · Cited by 9 · see citing works
Short-term effects of etifoxine on human gut microbiome in healthy men
Manook, A., Baghai, T. C., Riebel, M., Nothdurfter, C., Schwarzbach, J. V., Gessner, A., Rupprecht, R., & Hiergeist, A. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1188847 · Cited by 7 · see citing works
Neurological disorders associated with impaired gut microbiota
Kanhere, H. S., Rahangdale, Y. U., Bodele, A. S., Wadhwani, D. I., Ghoshewar, A. R., & Karande, S. P. (2021) · GSC Biological and Pharmaceutical Sciences · doi:10.30574/gscbps.2021.15.2.0121 · Cited by 5 · see citing works
Primary Structure of Glutamate Decarboxylase from E. coli
Maras, B., LUCA, E. D., Barra, D., Bossa, F., & John, R. A. (1991) · Elsevier eBooks · doi:10.1016/b978-0-08-040820-0.50016-9 · Cited by 3 · see citing works
The Gut Microbiome and the Central Nervous System (CNS)
Vijay, A., Ahmad, F., Sudesh, R., & Balakrishnan, A. (2024) · Springer eBooks · doi:10.1007/978-981-99-8803-7_3 · Cited by 2 · see citing works
The Microbiome in Neurogastroenterology
Preidis, G. A., Chumpitazi, B. P., & Shulman, R. J. (2016) · Springer eBooks · doi:10.1007/978-3-319-43268-7_5 · Cited by 2 · see citing works
Antifibrinolytics in Cardiac Surgery: What Is the Best Practice in 2022?
Strauss, E. R., Taneja, M., Booth, R., Sankova, S. K., & Anders, M. G. (2022) · Current anesthesiology reports · doi:10.1007/s40140-022-00538-w · Cited by 2 · see citing works
The Microbiome in Neurogastroenterology
Preidis, G. A., Chumpitazi, B. P., & Shulman, R. J. (2022) · Springer eBooks · doi:10.1007/978-3-031-15229-0_6 · Cited by 1 · see citing works
Tungland, B. C. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-814649-1.00012-0 · Cited by 1 · see citing works
Impact of the gut microbiome on human health and diseases
Banik, S. P., Sehgal, S., Ghosh, R. B., & Das, A. (2022) · Elsevier eBooks · doi:10.1016/b978-0-12-822238-6.00026-1 · Cited by 1 · see citing works
Chapter 17. Recent Developments in Cell Based Mechanism Screens
Gracheck, S. J., Miller, P. F., & Marks, J. S. (1993) · Annual reports in medicinal chemistry · doi:10.1016/s0065-7743(08)60887-8 · Cited by 1 · see citing works
Role of GABA Under Bacterial Stress in Plants
Lahry, K., Pandey, A. K., & Singh, S. (2025) · Wiley eBooks · doi:10.1002/9781394217786.ch15 · Cited by 1 · see citing works
Microbiota, the brain and epigenetics
Louwies, T., Johnson, A. C., Orock, A. M., Yuan, T., & Meerveld, B. G. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-816843-1.00026-6
Gut–brain communication: a novel application of probiotics
Das, S., Undhad, T. J., & Hati, S. (2022) · Elsevier eBooks · doi:10.1016/b978-0-12-822238-6.00017-0
Role of microbiota-gut-brain axis on neurotransmitter modulation
Anitha, K., Bhatt, S., Chikatipalli, R., & Ravula, P. (2025) · Elsevier eBooks · doi:10.1016/b978-0-443-21680-0.00016-x
Promoting Gut Microbiome Diversity in Anorexic Patients: A Neurobiological Review
Shankar, A., Wong, H., Kwe, I., & Wang, L. (2025) · Berkeley Pharma Tech Journal of Medicine · doi:10.52243/bptjm.v5i1.72
The ‘gut feeling’: Connecting neurodegenerative diseases and gut microbiota
Niyogi, S., & Basu, S. (2026) · The Microbe · doi:10.1016/j.microb.2026.100719
The gut–brain–epigenetic axis in brain health
Louwies, T. (2026) · Elsevier eBooks · doi:10.1016/b978-0-443-15572-7.00057-7
Escobar‐Salom, M., Barceló, I. M., Jordana‐Lluch, E., Sansó-Sastre, J., Lasarte-Monterrubio, C., Beceiro, A., Oliver, A., & Juan, C. (2026) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2026.1861295
- Authors
- Guthrie, G. D., & Nicholson-Guthrie, C. S.
- Affiliations
- Indiana University School of Medicine (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 1989-10
- Volume
- 86
- Issue
- 19
- Pages
- 7378-7381
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC298065
- OpenAlex
- W2088304943
- Cited by
- 61
- References
- 13
- Citations by year
- 2026: 3 · 2025: 4 · 2024: 3 · 2023: 2 · 2022: 7 · 2021: 3 · 2020: 3 · 2019: 6 · 2018: 3 · 2016: 3 · 2015: 1 · 2014: 2 · 2013: 1 · 2012: 4
- FWCI
- 0.27
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (2s07rr005371-30)
- National Center for Research Resources (5 S07 RR5371)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Amino Acid Enzymes and Metabolism
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Keywords
- GABA, GABA uptake, Pseudomonas fluorescens, neurotransmitter binding, GABA receptors, muscimol, sodium-independent transport, saturable binding, competitive inhibition
- MeSH terms
- Binding, Competitive, gamma-Aminobutyric Acid, Kinetics, Muscimol, Pseudomonas fluorescens, Receptors, GABA-A
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
