Trimethylamine and Trimethylamine N-Oxide, a Flavin-Containing Monooxygenase 3 (FMO3)-Mediated Host-Microbiome Metabolic Axis Implicated in Health and Disease

Fennema, Diede; Phillips, Ian R; Shephard, Elizabeth A

doi:10.1124/dmd.116.070615

Cited by 355Gut microbiota and healthPharmacogenetics and Drug MetabolismPolyamine Metabolism and Applications

Trimethylamine and Trimethylamine N-Oxide, a Flavin-Containing Monooxygenase 3 (FMO3)-Mediated Host-Microbiome Metabolic Axis Implicated in Health and Disease

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Fennema, Diede, Phillips, Ian R, Shephard, Elizabeth A·2016·Drug Metabolism and Disposition

DOI 10.1124/dmd.116.070615PMC PMC5074467

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Abstract

Flavin-containing monooxygenase 3 (FMO3) is known primarily as an enzyme involved in the metabolism of therapeutic drugs. On a daily basis, however, we are exposed to one of the most abundant substrates of the enzyme trimethylamine (TMA), which is released from various dietary components by the action of gut bacteria. FMO3 converts the odorous TMA to nonodorous TMA N-oxide (TMAO), which is excreted in urine. Impaired FMO3 activity gives rise to the inherited disorder primary trimethylaminuria (TMAU). Affected individuals cannot produce TMAO and, consequently, excrete large amounts of TMA. A dysbiosis in gut bacteria can give rise to secondary TMAU. Recently, there has been much interest in FMO3 and its catalytic product, TMAO, because TMAO has been implicated in various conditions affecting health, including cardiovascular disease, reverse cholesterol transport, and glucose and lipid homeostasis. In this review, we consider the dietary components that can give rise to TMA, the gut bacteria involved in the production of TMA from dietary precursors, the metabolic reactions by which bacteria produce and use TMA, and the enzymes that catalyze the reactions. Also included is information on bacteria that produce TMA in the oral cavity and vagina, two key microbiome niches that can influence health. Finally, we discuss the importance of the TMA/TMAO microbiome-host axis in health and disease, considering factors that affect bacterial production and host metabolism of TMA, the involvement of TMAO and FMO3 in disease, and the implications of the host-microbiome axis for management of TMAU.

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Approximately 50% of ingested TMAO is absorbed unchanged and excreted in urine; the remaining 50% is converted into TMA in the gut by TMAO reductase.
“Approximately 50% of the ingested TMAO is absorbed unchanged and then excreted in urine. The remaining 50% is converted into TMA in the gut by the action of TMAO reductase [19].”
From Implication of Trimethylamine N-Oxide (TMAO) in Disease: Potential Biomarker or New Therapeutic Target (2018) · cites this paper as [19]
Ergothioneine degradation by ergothionase produces TMA.
“The degradation of ergothioneine by the enzyme ergothionase produces TMA [19]”
From Implication of Trimethylamine N-Oxide (TMAO) in Disease: Potential Biomarker or New Therapeutic Target (2018) · cites this paper as [19]

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Macronutrient metabolism by the human gut microbiome: major fermentation by-products and their impact on host health
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The Gut Microbiota and Inflammation: An Overview
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“Interconversion of lecithin and choline is bidirectional, being the conversion of choline to lecithin catalysed by choline kinase [19] (Figure 1).”
BackgroundInfluential
Trace Amines and Their Receptors
Gainetdinov, R. R., Hoener, M. C., & Berry, M. D. (2018) · Pharmacological Reviews · doi:10.1124/pr.117.015305 · Cited by 389 · see citing works
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Diversity of vaginal microbiome and metabolome during genital infections
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TMAO: how gut microbiota contributes to heart failure
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The role of intestinal microbiota in cardiovascular disease
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Pharmacology of human trace amine-associated receptors: Therapeutic opportunities and challenges
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Gut Microbiota-Derived Components and Metabolites in the Progression of Non-Alcoholic Fatty Liver Disease (NAFLD)
Ji, Y. S., Yin, Y., Li, Z., & Zhang, W. (2019) · Nutrients · doi:10.3390/nu11081712 · Cited by 230 · see citing works
Trimethylamine N-Oxide Generated by the Gut Microbiota Is Associated with Vascular Inflammation: New Insights into Atherosclerosis
Liu, Y., & Dai, M. (2020) · Mediators of Inflammation · doi:10.1155/2020/4634172 · Cited by 231 · see citing works
Trimethylamine N-oxide (TMAO) in human health
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Metabolite interactions between host and microbiota during health and disease: Which feeds the other?
Zhang, Y., Chen, R., Zhang, D., Qi, S., & Liu, Y. (2023) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2023.114295 · Cited by 209 · see citing works
Effect of Berberine on Atherosclerosis and Gut Microbiota Modulation and Their Correlation in High-Fat Diet-Fed ApoE−/− Mice
Wu, M., Yang, S., Wang, S., Cao, Y., Zhao, R., Li, X., Xing, Y., & Liu, L. (2020) · Frontiers in Pharmacology · doi:10.3389/fphar.2020.00223 · Cited by 201 · see citing works
Gut microbiota in atherosclerosis: focus on trimethylamine N‐oxide
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Gut Microbiota-Dependent Trimethylamine-N-oxide and Serum Biomarkers in Patients with T2DM and Advanced CKD
Al-Obaide, M. A. I., Singh, R., Datta, P., Rewers-Felkins, K., Salguero, M. V., Al‐Obaidi, I., Kottapalli, K. R., & Vasylyeva, T. L. (2017) · Journal of Clinical Medicine · doi:10.3390/jcm6090086 · Cited by 200 · see citing works
Host-microbiome interactions: Gut-Liver axis and its connection with other organs
Anand, S., & Mande, S. S. (2022) · npj Biofilms and Microbiomes · doi:10.1038/s41522-022-00352-6 · Cited by 196 · see citing works
Gut microbiota metabolites, amino acid metabolites and improvements in insulin sensitivity and glucose metabolism: the POUNDS Lost trial
Heianza, Y., Sun, D., Li, X., DiDonato, J. A., Bray, G. A., Sacks, F. M., & Qi, L. (2019) · Gut · doi:10.1136/gutjnl-2018-316155 · Cited by 177 · see citing works
Interactions between gut microbiota and polyphenols: A mechanistic and metabolomic review
Cheng, H., Zhang, D., Wu, J., Liu, J., Zhou, Y., Tan, Y., Feng, W., & Peng, C. Y. (2023) · Phytomedicine · doi:10.1016/j.phymed.2023.154979 · Cited by 188 · see citing works
Trimethylamine N‐oxide: breathe new life
Subramaniam, S., & Fletcher, C. (2018) · British Journal of Pharmacology · doi:10.1111/bph.13959 · Cited by 171 · see citing works
Interaction between gut microbiome and cardiovascular disease
Peng, J., Xiao, X., Hu, M., & Zhang, X. (2018) · Life Sciences · doi:10.1016/j.lfs.2018.10.063 · Cited by 175 · see citing works
Associations of plasma trimethylamine N-oxide, choline, carnitine, and betaine with inflammatory and cardiometabolic risk biomarkers and the fecal microbiome in the Multiethnic Cohort Adiposity Phenotype Study
Fu, B. C., Hullar, M. A. J., Randolph, T. W., Franke, A. A., Monroe, K. R., Cheng, I. C., Wilkens, L. R., Shepherd, J., Madeleine, M. M., Marchand, L. L., et al. (2020) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/nqaa015 · Cited by 171 · see citing works
Total volatile basic nitrogen and trimethylamine in muscle foods: Potential formation pathways and effects on human health
Bekhit, A. E. A., Giteru, S. G., Holman, B. W. B., & Hopkins, D. L. (2021) · Comprehensive Reviews in Food Science and Food Safety · doi:10.1111/1541-4337.12764 · Cited by 169 · see citing works
Flavin monooxygenase 3, the host hepatic enzyme in the metaorganismal trimethylamine N‐oxide‐generating pathway, modulates platelet responsiveness and thrombosis risk
Zhu, W., Buffa, J. A., Wang, Z., Warrier, M., Schugar, R., Shih, D. M., Gupta, N., Gregory, J. C., Org, E., Fu, X., et al. (2018) · Journal of Thrombosis and Haemostasis · doi:10.1111/jth.14234 · Cited by 161 · see citing works
An obesity-associated gut microbiome reprograms the intestinal epigenome and leads to altered colonic gene expression
Qin, Y., Roberts, J. D., Grimm, S. A., Lih, F. B., Deterding, L. J., Li, R., Chrysovergis, K., & Wade, P. A. (2018) · Genome biology · doi:10.1186/s13059-018-1389-1 · Cited by 161 · see citing works
Gut Microbiota Dysbiosis and Increased Plasma LPS and TMAO Levels in Patients With Preeclampsia
Wang, J., Gu, X., Yang, J., Wei, Y., & Zhao, Y. (2019) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2019.00409 · Cited by 161 · see citing works
The Epigenetic Connection Between the Gut Microbiome in Obesity and Diabetes
Sharma, M., Li, Y., Stoll, M. L., & Tollefsbol, T. O. (2020) · Frontiers in Genetics · doi:10.3389/fgene.2019.01329 · Cited by 152 · see citing works
Trimethylamine N-Oxide in Relation to Cardiometabolic Health—Cause or Effect?
Papandreou, C., Moré, M. I., & Bellamine, A. (2020) · Nutrients · doi:10.3390/nu12051330 · Cited by 150 · see citing works
Interactions between gut microbiota and berberine, a necessary procedure to understand the mechanisms of berberine
Cheng, H., Liu, J., Tan, Y., Feng, W., & Peng, C. Y. (2021) · Journal of Pharmaceutical Analysis · doi:10.1016/j.jpha.2021.10.003 · Cited by 137 · see citing works
Gut microbiota derived metabolites contribute to intestinal barrier maturation at the suckling-to-weaning transition
Beaumont, M., Paës, C., Mussard, E., Knudsen, C., Cauquil, L., Aymard, P., Barilly, C., Gabinaud, B., Zemb, O., Fourré, S., et al. (2020) · Gut Microbes · doi:10.1080/19490976.2020.1747335 · Cited by 145 · see citing works
Trimethylamine N-oxide, Mediterranean diet, and nutrition in healthy, normal-weight adults: also a matter of sex?
Barrea, L., Annunziata, G., Muscogiuri, G., Laudisio, D., Somma, C. D., Maisto, M., Tenore, G. C., Colao, A., & Savastano, S. (2018) · Nutrition · doi:10.1016/j.nut.2018.11.015 · Cited by 131 · see citing works
Trimethylamine N -oxide: A harmful, protective or diagnostic marker in lifestyle diseases?
Nowiński, A., & Ufnal, M. (2017) · Nutrition · doi:10.1016/j.nut.2017.08.001 · Cited by 130 · see citing works
Fructus Ligustri Lucidi preserves bone quality through the regulation of gut microbiota diversity, oxidative stress, TMAO and Sirt6 levels in aging mice
Li, L., Chen, B., Zhu, R., Li, R., Tian, Y., Liu, C., Jia, Q., Wang, L., Tang, J., Zhao, D., et al. (2019) · Aging · doi:10.18632/aging.102376 · Cited by 128 · see citing works
l ‐lysine metabolism to N‐hydroxypipecolic acid: an integral immune‐activating pathway in plants
Hartmann, M., & Zeier, J. (2018) · The Plant Journal · doi:10.1111/tpj.14037 · Cited by 126 · see citing works
Understanding the Effects of Gut Microbiota Dysbiosis on Nonalcoholic Fatty Liver Disease and the Possible Probiotics Role: Recent Updates
Khan, A., Ding, Z., Ishaq, M. H., Bacha, A. S., KHAN, I. A., Hanif, A., Li, W., & Guo, X. (2021) · International Journal of Biological Sciences · doi:10.7150/ijbs.56214 · Cited by 126 · see citing works
Dietary bioactive ingredients to modulate the gut microbiota-derived metabolite TMAO. New opportunities for functional food development
Simó, C., & García‐Cañas, V. (2020) · Food & Function · doi:10.1039/d0fo01237h · Cited by 110 · see citing works
The Role of a Gut Microbial-Derived Metabolite, Trimethylamine N-Oxide (TMAO), in Neurological Disorders
Praveenraj, S. S., Sonali, S., Anand, N., Hediyal, T. A., Vichitra, C., Kalyan, M., Kanna, P. V., Chandana, K. A., Paneyala, S., Mahalakshmi, A. M., et al. (2022) · Molecular Neurobiology · doi:10.1007/s12035-022-02990-5 · Cited by 111 · see citing works
Effects of Grape Pomace Polyphenolic Extract (Taurisolo®) in Reducing TMAO Serum Levels in Humans: Preliminary Results from a Randomized, Placebo-Controlled, Cross-Over Study
Annunziata, G., Maisto, M., Schisano, C., Ciampaglia, R., Narciso, V., Tenore, G. C., & Novellino, E. (2019) · Nutrients · doi:10.3390/nu11010139 · Cited by 107 · see citing works
Associations of dietary choline intake with risk of incident dementia and with cognitive performance: the Kuopio Ischaemic Heart Disease Risk Factor Study
Ylilauri, M. P., Voutilainen, S., Lönnroos, E., Virtanen, H. E., Tuomainen, T., Salonen, J. T., & Virtanen, J. K. (2019) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/nqz148 · Cited by 106 · see citing works
Factors shaping the abundance and diversity of the gut archaeome across the animal kingdom
Thomas, C. M., Quéméner, E. D., Gribaldo, S., & Borrel, G. (2022) · Nature Communications · doi:10.1038/s41467-022-31038-4 · Cited by 104 · see citing works
Plant-Based Diets in the Reduction of Body Fat: Physiological Effects and Biochemical Insights
Najjar, R. S., & Feresin, R. G. (2019) · Nutrients · doi:10.3390/nu11112712 · Cited by 100 · see citing works
A microbial transporter of the dietary antioxidant ergothioneine
Dumitrescu, D. G., Gordon, E. M., Kovalyova, Y., Seminara, A. B., Lowey, B., Forster, E. R., Zhou, W., Booth, C. J., Shen, A., Kranzusch, P. J., et al. (2022) · Cell · doi:10.1016/j.cell.2022.10.008 · Cited by 99 · see citing works
Implications of the Intestinal Microbiota in Diagnosing the Progression of Diabetes and the Presence of Cardiovascular Complications
Leustean, A. M., Ciocoiu, M., Sava, A. C., Costea, C. F., Floria, M., Tărniceriu, C. C., & Tănase, D. M. (2018) · Journal of Diabetes Research · doi:10.1155/2018/5205126 · Cited by 92 · see citing works
The gut microbiota derived metabolite trimethylamine N-oxide: Its important role in cancer and other diseases
Zhou, Y., Zhang, Y., Jin, S., Lv, J., Li, M., & Feng, N. (2024) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2024.117031 · Cited by 92 · see citing works
Gut Microbial Metabolites and Blood Pressure Regulation: Focus on SCFAs and TMAO
Poll, B. G., Cheema, M. U., & Pluznick, J. L. (2020) · Physiology · doi:10.1152/physiol.00004.2020 · Cited by 84 · see citing works
Hepatic Lipid Metabolism Disorder and Atherosclerosis
Zhang, S., Hong, F., Ma, C., & Yang, S. (2021) · Endocrine Metabolic & Immune Disorders - Drug Targets · doi:10.2174/1871530322666211220110810 · Cited by 83 · see citing works
The Fibrotic Effects of TMAO on Human Renal Fibroblasts Is Mediated by NLRP3, Caspase-1 and the PERK/Akt/mTOR Pathway
Kapetanaki, S., Kumawat, A. K., Persson, K., & Demirel, I. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222111864 · Cited by 80 · see citing works
Trimethylamine-N-Oxide (TMAO) as a Rising-Star Metabolite: Implications for Human Health
Caradonna, E., Abate, F., Schiano, E., Paparella, F., Ferrara, F., Vanoli, E., Difruscolo, R., Goffredo, V. M., Amato, B., Setacci, C., et al. (2025) · Metabolites · doi:10.3390/metabo15040220 · Cited by 88 · see citing works
Chemotherapy-induced gastrointestinal toxicity is associated with changes in serum and urine metabolome and fecal microbiota in male Sprague–Dawley rats
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The roles of trimethylamine-N-oxide in atherosclerosis and its potential therapeutic aspect: A literature review
Oktaviono, Y. H., Lamara, A. D., Saputra, P. B. T., Arnindita, J. N., Pasahari, D., Saputra, M. E., & Suasti, N. M. A. (2023) · Biomolecules and Biomedicine · doi:10.17305/bb.2023.8893 · Cited by 87 · see citing works
Trimethylamine N -oxide: heart of the microbiota–CVD nexus?
Naghipour, S., Cox, A. J., Peart, J. N., Toit, E. F. D., & Headrick, J. P. (2020) · Nutrition Research Reviews · doi:10.1017/s0954422420000177 · Cited by 75 · see citing works
Role of the Gut Microbiome in the Development of Atherosclerotic Cardiovascular Disease
Samarraie, A. A., Pichette, M., & Rousseau, G. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24065420 · Cited by 76 · see citing works
Puerarin alleviates atherosclerosis via the inhibition of Prevotella copri and its trimethylamine production
Li, Z. H. (2024) · Gut · doi:10.1136/gutjnl-2024-331880 · Cited by 76 · see citing works
Flavin-containing monooxygenase 3 (FMO3): genetic variants and their consequences for drug metabolism and disease
Phillips, I. R., & Shephard, E. A. (2019) · Xenobiotica · doi:10.1080/00498254.2019.1643515 · Cited by 71 · see citing works
Self-citation
The Microbial Metabolite Trimethylamine N-Oxide Links Vascular Dysfunctions and the Autoimmune Disease Rheumatoid Arthritis
Chan, M. M.-Y., Yang, X., Wang, H., Saaoud, F., Sun, Y., & Fong, D. (2019) · Nutrients · doi:10.3390/nu11081821 · Cited by 68 · see citing works
The Brain–Gut Axis, an Important Player in Alzheimer and Parkinson Disease: A Narrative Review
Caradonna, E., Nemni, R., Bifone, A., Gandolfo, P., Costantino, L., Giordano, L., Mormone, E., Macula, A., Cuomo, M., Difruscolo, R., et al. (2024) · Journal of Clinical Medicine · doi:10.3390/jcm13144130 · Cited by 75 · see citing works
Trimethylamine N-Oxide and Cardiovascular Outcomes in Patients with ESKD Receiving Maintenance Hemodialysis
Stubbs, J. R., Stedman, M. R., Liu, S., Long, J., Franchetti, Y., West, R. E., Prokopienko, A. J., Mahnken, J. D., Chertow, G. M., & Nolin, T. D. (2019) · Clinical Journal of the American Society of Nephrology · doi:10.2215/cjn.06190518 · Cited by 68 · see citing works
Trimethylamine N-Oxide Metabolites in Early Pregnancy and Risk of Gestational Diabetes: A Nested Case-Control Study
Huo, X., Li, J., Cao, Y., Li, S., Shao, P., Leng, J., Li, W., Liu, J., Yang, K., Ronald, C. W., et al. (2019) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2019-00710 · Cited by 65 · see citing works
Multi‐compartment metabolomics and metagenomics reveal major hepatic and intestinal disturbances in cancer cachectic mice
Pötgens, S. A., Thibaut, M. M., Joudiou, N., Sboarina, M., Neyrinck, A. M., Cani, P. D., Claus, S. P., Delzenne, N. M., & Bindels, L. B. (2021) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1002/jcsm.12684 · Cited by 67 · see citing works
Targeting Trimethylamine N-Oxide: A New Therapeutic Strategy for Alleviating Atherosclerosis
Jing, L., Zhang, H., Xiang, Q., Shen, L., Guo, X., Zhai, C., & Hu, H. (2022) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2022.864600 · Cited by 66 · see citing works
The use of an in-vitro batch fermentation (human colon) model for investigating mechanisms of TMA production from choline, l-carnitine and related precursors by the human gut microbiota
Day-Walsh, P. E., Shehata, E., Saha, S., Savva, G. M., Nemeckova, B., Speranza, J., Kellingray, L., Narbad, A., & Kroon, P. A. (2021) · European Journal of Nutrition · doi:10.1007/s00394-021-02572-6 · Cited by 61 · see citing works
Balancing the Equation: A Natural History of Trimethylamine and Trimethylamine-N-oxide
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Authors: Fennema, D., Phillips, I. R., & Shephard, E. A.
Affiliations: Queen Mary University of London (GB)
Corresponding author: Shephard, Elizabeth A
ORCID: Fennema, Diede
Phillips, Ian R
Shephard, Elizabeth A
Venue: Drug Metabolism and Disposition
Publisher: Elsevier BV
Published: 2016-11
Volume: 44
Issue: 11
Pages: 1839-1850
ISSN: 0090-9556 (ISSN-L)
DOI: 10.1124/dmd.116.070615
PMC: PMC5074467
OpenAlex: W2397682060
Cited by: 355
References: 192
Citations by year: 2026: 22 · 2025: 39 · 2024: 48 · 2023: 30 · 2022: 36 · 2021: 56 · 2020: 52 · 2019: 36 · 2018: 20 · 2017: 15
FWCI: 2.14
Type: journal article
Language: en
Update notices: erratum (2016-12-01)
Open access: hybrid
doi.org
Licence: cc-by
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
creativecommons.org/licenses/by/4.0/ (vor, 2983 d)
Locations: Drug Metabolism and Disposition (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by-nc)
PubMed (publishedVersion)
UCL Discovery (University College London) (submittedVersion)
Funders: Medical Research Council (MR/K015494/1)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Life Sciences › Pharmacology, Toxicology and Pharmaceutics › Pharmacology › Pharmacogenetics and Drug Metabolism
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Polyamine Metabolism and Applications
Keywords: trimethylamine, trimethylamine N-oxide, FMO3, trimethylaminuria, gut microbiota, dietary precursors, oral microbiota, vaginal microbiota, cardiovascular disease, reverse cholesterol transport, glucose and lipid homeostasis
MeSH terms: Gastrointestinal Microbiome, Animals, Cardiovascular Diseases, Humans, Methylamines, Oxygenases, Host-Pathogen Interactions

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Trimethylamine and Trimethylamine N-Oxide, a Flavin-Containing Monooxygenase 3 (FMO3)-Mediated Host-Microbiome Metabolic Axis Implicated in Health and Disease

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