Carnitine metabolism to trimethylamine by an unusual Rieske-type oxygenase from human microbiota
Open accessAbstract
Significance: Metabolism of l -carnitine, a compound abundant in human diet, to trimethylamine by human microbiota has been shown to promote atherosclerosis and subsequent development of heart disease. However, the underpinning molecular and biochemical mechanisms remain unknown. In this study, we reveal that a previously unidentified Rieske-type protein is responsible for carnitine transformation to trimethylamine from human microbiota. Knowledge gained in our study provides the opportunity not only to explore Rieske protein inhibitors in preventing trimethylamine formation in animal studies and clinical trials, but also for its use as a functional genetic marker to better understand human microbiota and their dynamics in our health and disease in future epidemiological studies and dietary interventions.
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Gut microbes possess TMA lyases that cleave the C-N bond of choline/phosphatidylcholine and carnitine, releasing TMA.
“While mammals do not have the enzyme, gut microbes have TMA lyases, which can cleave the C-N bond of these nutrients, releasing the TMA moiety as a waste product.”
From The contributory role of gut microbiota in cardiovascular disease (2014) · cites this paper as [77]
Two distinct microbial enzyme systems have been identified in vitro that can produce TMA from either choline or carnitine.
“Thus far, 2 distinct microbial enzyme systems have been identified in vitro that can produce TMA from either choline or carnitine as substrate (75,77).”
From The contributory role of gut microbiota in cardiovascular disease (2014) · cites this paper as [77]
The microbial oxygenase CntA complexes with the reductase CntB to form an active complex that selectively uses carnitine and forms TMA, producing carnitine TMA lyase activity.
“Similarly, a microbial oxygenase (CntA) complexes with the microbial reductase (CntB) to form an active complex that selectively uses carnitine as substrate and forms TMA (carnitine TMA lyase activity).”
From The contributory role of gut microbiota in cardiovascular disease (2014) · cites this paper as [77]
Recombinant isolated CntA/B formed a two-component Rieske-type oxygenase/reductase complex.
“Characterization of recombinant isolated CntA/B showed they formed a 2-component Rieske-type oxygenase/reductase complex (77).”
From The contributory role of gut microbiota in cardiovascular disease (2014) · cites this paper as [77]
Using Acinetobacter baumannii as a model, an alternative microbial enzyme cluster CntA and CntB specific for carnitine TMA lyase activity was reported.
“In other studies that used a similar bioinformatics approach with Acinetobacter baumannii as the model, an alternative microbial enzyme cluster (catalytic and regulatory protein CntA and CntB) specific for carnitine TMA lyase activity was also recently reported (77).”
From The contributory role of gut microbiota in cardiovascular disease (2014) · cites this paper as [77]
L-carnitine is converted into TMA mainly by carnitine oxidoreductase.
“Carnitine oxidoreductase is the main enzyme responsible for the conversion of L-carnitine into TMA [20]”
From Implication of Trimethylamine N-Oxide (TMAO) in Disease: Potential Biomarker or New Therapeutic Target (2018) · cites this paper as [20]
CntA and CntB encode a two-subunit oxidoreductase that converts L-carnitine to TMA.
“Two genes, CntA and CntB, encode a two-subunit oxidoreductase (A encodes the carnitine oxidase, and B encodes a reductase) for L-carnitine conversion to TMA (confirmed by a series of knockout and heterologous expression experiments) (137).”
From Trimethylamine <i>N</i> -Oxide, the Microbiome, and Heart and Kidney Disease (2017) · cites this paper as [137]
TMA is produced by carnitine oxygenase using carnitine found in red meat as a substrate.
“TMA is also produced by carnitine oxygenase, a Rieske-type protein, using carnitine found in red meat as a substrate (Zhu et al., 2014).”
From Gut reactions: Breaking down xenobiotic–microbiome interactions (2019) · cites this paper as Zhu et al., 2014
Two major TMA-synthesis pathways have been described: CutC/CutD takes choline as substrate, and CntA/B acts on carnitine and gamma-butyrobetaine.
“Two major TMA-synthesis pathways have been described with a specific glycyl radical enzyme, the choline TMA-lyase (CutC) and its activator CutD [6], that takes choline as a substrate and a two-component Rieske-type oxygenase/reductase (CntA/B) [7], which acts on carnitine and its derivative gamma-butyrobetaine, as the key enzymes.”
From Uncovering the trimethylamine-producing bacteria of the human gut microbiota (2017) · cites this paper as [7]
In this study, YeaW was considered as belonging to the CntA cluster of enzymes as originally proposed by Zhu and colleagues.
“In this study, we, hence, considered YeaW as belonging to the CntA cluster of enzymes as originally proposed by Zhu and colleagues [7].”
From Uncovering the trimethylamine-producing bacteria of the human gut microbiota (2017) · cites this paper as [7]
All cntA sequences, with one exception, display a conserved bridging glutamate instead of aspartate (E205D), previously suggested as a signature for that enzyme.
“All sequences (with one exception) display a conserved “bridging” glutamate instead of aspartate (E205D), which was previously suggested as a signature for that enzyme [7].”
From Uncovering the trimethylamine-producing bacteria of the human gut microbiota (2017) · cites this paper as [7]
The established databases present a comprehensive update of previous cutC and cntA gene sequence collections, adding a multitude of new gene sequences.
“The established databases present a comprehensive update of previous cutC [9] and cntA [7] gene sequence collections adding a multitude of new gene sequences.”
From Uncovering the trimethylamine-producing bacteria of the human gut microbiota (2017) · cites this paper as [7]
TMA formation via cntA represents a distinctive branch of TMA synthesis.
“TMA formation via cntA represents a distinctive branch of TMA synthesis”
From Uncovering the trimethylamine-producing bacteria of the human gut microbiota (2017) · cites this paper as [7]
Specific conditions that select against cutC-containing bacteria might be compensated by an increase of taxa encoding CntA.
“Thus, specific conditions that select against the latter bacteria might be compensated by an increase of taxa encoding CntA [7]”
From Uncovering the trimethylamine-producing bacteria of the human gut microbiota (2017) · cites this paper as [7]
Ecophysiologic features of E. coli, the key player of cntA, are substantially different to those of the major cutC-exhibiting taxa.
“ecophysiologic features of its key player, E. coli, are substantially different to those of the major cutC-exhibiting taxa”
From Uncovering the trimethylamine-producing bacteria of the human gut microbiota (2017) · cites this paper as [7]
Human and animal studies suggest that several families of bacteria are involved in TMA/TMAO production, namely Deferribacteraceae, Anaeroplasmataceae, Prevotellaceae and Enterobacteriaceae.
“Human and animal studies suggest that several families of bacteria are involved in TMA/TMAO production, namely, Deferribacteraceae, Anaeroplasmataceae, Prevotellaceae [3] and Enterobacteriaceae [18,19].”
From Trimethylamine N-oxide: the good, the bad and the unknown. (2016) · cites this paper as [19]
In the MEDIT-AHF study, patients had decreased risk for rehospitalization.
“However, the patients did have decreased risk for rehospitalization.”
From Dietary metabolism, the gut microbiome, and heart failure (2019) · cites this paper as [224]
In the MEDIT-AHF study, there were no long-term benefits in mortality.
“the authors did not see long-term benefits in mortality224.”
From Dietary metabolism, the gut microbiome, and heart failure (2019) · cites this paper as [224]
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“Carnitine oxidoreductase is the main enzyme responsible for the conversion of L-carnitine into TMA [20] (Figure 1).”
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Self-citation
- Authors
- Zhu, Y., Jameson, E., Crosatti, M., Schäfer, H., Rajakumar, K., Bugg, T. D. H., & Chen, Y.
- Affiliations
- School of Life Sciences and
- University of Leicester (GB)
- University of Warwick (GB)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2014-03-03
- Volume
- 111
- Issue
- 11
- Pages
- 4268-4273
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3964110
- OpenAlex
- W2000670099
- Cited by
- 372
- References
- 58
- Citations by year
- 2026: 22 · 2025: 35 · 2024: 46 · 2023: 36 · 2022: 44 · 2021: 47 · 2020: 36 · 2019: 22 · 2018: 29 · 2017: 14 · 2016: 16 · 2015: 17 · 2014: 7
- FWCI
- 7.34
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Warwick Research Archive Portal (University of Warwick) (acceptedVersion)
- University of Birmingham Research Portal (University of Birmingham) (submittedVersion)
- Funders
- Royal Society
- Natural Environment Research Council (NE/I027061/1)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial metabolism and enzyme function
- Physical Sciences › Chemistry › Inorganic Chemistry › Metal-Catalyzed Oxygenation Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Polyamine Metabolism and Applications
- Keywords
- carnitine metabolism, trimethylamine, human gut microbiome, Acinetobacter baumannii, heterologous expression, trimethylamine N-oxide, cardiovascular disease, flavin-containing monooxygenase, gene clusters
- MeSH terms
- Carnitine, Chromatography, Ion Exchange, Escherichia coli, Humans, Methylamines, Oxidoreductases, Oxygenases, Spectrophotometry, Ultraviolet, Mutagenesis, Site-Directed, Computational Biology, Acinetobacter baumannii, Microbiota
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