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1 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 bioRxiv preprint doi: https://doi.org/10.1101/225581; this version posted December 11, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Metabolic retroconversion of trimethylamine N-oxide and the gut microbiota 2 3 Lesley Hoyles1*, Maria L. Jiménez-Pranteda2*, Julien Chilloux1*, Francois Brial3, Antonis 4 Myridakis1, Thomas Aranias3, Christophe Magnan4, Glenn R. Gibson2, Jeremy D. Sanderson5, Jeremy 5 K. Nicholson1, Dominique Gauguier1,3, Anne L. McCartney2† and Marc-Emmanuel Dumas1† 6 7 1Integrative Systems Medicine and Digestive Disease, Department of Surgery and Cancer, Faculty of 8 Medicine, Imperial College London, Exhibition Road, London SW7 2AZ, UK 9 2Food Microbial Sciences Unit, Department of Food and Nutritional Sciences, School of Chemistry, 10 Food and Pharmacy, Faculty of Life Sciences, The University of Reading, Whiteknights Campus, 11 Reading RG6 6UR, UK 12 3Sorbonne Universities, University Pierre & Marie Curie, University Paris Descartes, Sorbonne Paris 13 Cité, INSERM UMR_S 1138, Cordeliers Research Centre, Paris, France 14 4Sorbonne Paris Cité, Université Denis Diderot, Unité de Biologie Fonctionnelle et Adaptative, CNRS 15 UMR 8251, 75205 Paris, France 16 5Department of Gastroenterology, Guy's and St Thomas' NHS Foundation Trust and King's College 17 London, London, UK 18 19 *These authors made equal contributions to this work; shared first authorship. 20 †Corresponding authors: Anne L. McCartney, [email protected]; Marc-Emmanuel 21 Dumas, [email protected] 22 23 Running title: Reduction of TMAO by the human gut microbiota 24 Abbreviations: AUC, area under the curve; DMA, dimethylamine; FISH, fluorescence in situ 25 hybridization; FMO, flavin mono-oxygenase; MMA, monomethylamine; PC, phosphatidylcholine; 26 TMA, trimethylamine; TMAO, trimethylamine N-oxide; UPLC–MS/MS, ultra-performance liquid 27 chromatography–tandem mass spectrometry. 28 Keywords: co-metabolic axis; gut–liver axis; metabolomics; Enterobacteriaceae; lactic acid bacteria. 1 bioRxiv preprint doi: https://doi.org/10.1101/225581; this version posted December 11, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 29 ABSTRACT 30 The dietary methylamines choline, carnitine and phosphatidylcholine are used by the gut microbiota 31 to produce a range of metabolites, including trimethylamine (TMA). However, little is known about 32 the use of trimethylamine N-oxide (TMAO) by this consortium of microbes. A feeding study using 33 deuterated TMAO in C57BL6/J mice demonstrated microbial conversion of TMAO to TMA, with 34 uptake of TMA into the bloodstream and its conversion to TMAO. Antibiotic-treated mice lacked 35 microbial activity necessary to convert TMAO to TMA, with deuterated TMAO being taken up 36 directly into the bloodstream. In batch-culture fermentation systems inoculated with human faeces, 37 growth of Enterobacteriaceae was stimulated in the presence of TMAO. Human-derived faecal and 38 caecal bacteria (n = 66 isolates) were screened on solid and liquid media for their ability to use 39 TMAO, with metabolites in spent media analysed by 1H-NMR. As with the in vitro fermentation 40 experiments, TMAO stimulated the growth of Enterobacteriaceae; these bacteria produced most 41 TMA from TMAO. Caecal/small intestinal isolates of Escherichia coli produced more TMA from 42 TMAO than their faecal counterparts. Lactic acid bacteria produced increased amounts of lactate 43 when grown in the presence of TMAO, but did not produce large amounts of TMA. In summary, 44 TMA can be produced by the gut microbiota (predominantly Enterobacteriaceae) from TMAO. This 45 TMA is then taken up by the host and converted back to TMAO. That is, metabolic retroconversion 46 occurs. In addition, TMAO influences microbial metabolism depending on isolation source and taxon 47 of gut bacterium. 48 2 bioRxiv preprint doi: https://doi.org/10.1101/225581; this version posted December 11, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 49 INTRODUCTION 50 Dietary methylamines such as choline, trimethylamine N-oxide (TMAO), 51 phosphatidylcholine (PC) and carnitine are present in a number of foodstuffs, including meat, fish, 52 nuts and eggs. It has long been known that gut bacteria are able to use choline in a fermentation-like 53 process, with trimethylamine (TMA), ethanol, acetate and ATP among the known main end-products 54 (Wünsche, 1940; Bradbeer, 1965; Zeisel et al., 1983). TMA can be used by members of the order 55 Methanomassiliicoccales (Archaea) present in the human gut to produce methane (Borrel et al., 56 2017), or taken up by the host. Microbially produced TMA derived from PC is absorbed in the small 57 intestine (Stremmel et al., 2017). TMA diffuses into the bloodstream from the intestine via the hepatic 58 vein to hepatocytes, where it is converted to trimethylamine N-oxide (TMAO) by hepatic flavin- 59 containing mono-oxygenases (FMOs; Bennett et al., 2013). The bulk of TMAO, and lesser amounts 60 of TMA, derived from dietary methylamines can be detected in urine within 6 h of ingestion, and both 61 compounds are excreted in urine but not faeces (de la Huerga and Popper, 1951; Taesuwan et al., 62 2017). TMAO can also be detected in human skeletal muscle within 6 h of an oral dose of TMAO 63 (Taesuwan et al., 2017). 64 TMAO present in urine and plasma is considered a biomarker for non-alcoholic fatty liver 65 disease (NAFLD), insulin resistance and cardiovascular disease (Dumas et al., 2006; Spencer et al., 66 2011; Tang et al., 2013; Dumas et al., 2017). Feeding TMAO to high-fat-fed C57BL/6 mice 67 exacerbates impaired glucose tolerance, though the effect on the gut microbiota is unknown (Gao et 68 al., 2014). Low plasma PC and high urinary methylamines (including TMAO) were observed in 69 insulin-resistant mice on a high-fat diet, suggesting microbial methylamine metabolism directly 70 influences choline bioavailability (Dumas et al., 2006), and choline bioavailability is known to 71 contribute to hepatic steatosis in patients (Spencer et al., 2011). High levels of circulating TMAO are 72 associated with cardiovascular disease (Tang et al., 2013). However, circulating TMAO has been 73 suggested to play a role in protection from hyperammonemia, acting as an osmoprotectant, and from 74 glutamate neurotoxicity (Kloiber et al., 1988; Miñana et al., 1996). Recently, chronic exposure to 75 TMAO has been shown to attenuate diet-associated impaired glucose tolerance in mice, and reduce 76 endoplasmic reticulum stress and adipogenesis in adipocytes (Dumas et al., 2017). There is a basal 3 bioRxiv preprint doi: https://doi.org/10.1101/225581; this version posted December 11, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 77 level of TMA and TMAO detected in human urine even in the absence of dietary supplementation (de 78 la Huerga et al., 1953), suggesting use of (microbial and/or host) cell-derived choline or PC in the 79 intestinal tract by the gut microbiota. 80 While it is well established that choline (Zeisel et al., 1983; Wang et al., 2011; Spencer et al., 81 2011), PC (Zeisel et al., 1983; Tang et al., 2013) and carnitine (Rebouche et al., 1984; Seim et al., 82 1985; Rebouche and Chenard, 1991; Koeth et al., 2013) are used by the human and rodent gut 83 microbiotas to produce TMA, little is known about the reduction of TMAO (predominantly from fish) 84 to TMA (or other compounds) by members of these consortia. TMAO is found at concentrations of 85 20–120 mg per 100 g fish fillet (Jebsen and Riaz, 1977). Ingestion of fish by humans leads to 86 increased urinary excretion of dimethylamine (DMA) and TMA, from 5.6 to 24.1 and from 0.2 to 1.6 87 µmol/24 h/kg of body weight, respectively (Zeisel and Da Costa, 1986). Individuals with 88 trimethylaminuria (fish odour syndrome), in which TMA is not detoxified to TMAO by hepatic 89 FMOs, have been shown to reduce 40–60 % of an oral dose of TMAO to TMA (al-Waiz et al., 1987). 90 It was suggested the gut microbiota was responsible for reducing TMAO in these individuals, and in 91 those individuals without trimethylaminuria the TMA was re-oxidized in the liver before being 92 excreted in the urine. The process was termed ‘metabolic retroversion’ “(i.e., a cycle of reductive 93 followed by oxidative reactions to regenerate TMAO)” (al-Waiz et al., 1987). The reduction of 94 TMAO to TMA is most commonly associated with the gut microbiota of marine fish, with the TMA 95 generated by these bacteria contributing to the characteristic odour of rotting fish (Barrett and Kwan, 96 1985). Members of the class Gammaproteobacteria, which includes a number of food spoilage 97 organisms, are known to reduce TMAO to TMA quantitatively and are unable to reduce TMA further 98 (Takagi and Ishimoto, 1983; Barrett and Kwan, 1985). The conversion of TMAO to TMA by bacteria 99 represents a unique form of anaerobic respiration, in which TMAO reductase acts as a terminal 100 electron acceptor (from NADH or formate) for respiratory electron flow (Takagi and Ishimoto, 1983).
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