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Tungsten enzymes play a role in detoxifying food and antimicrobial aldehydes in the human gut microbiome.

ABSTRACT: Tungsten (W) is a metal that is generally thought to be seldom used in biology. We show here that a W-containing oxidoreductase (WOR) family is diverse and widespread in the microbial world. Surprisingly, WORs, along with the tungstate-specific transporter Tup, are abundant in the human gut microbiome, which contains 24 phylogenetically distinct WOR types. Two model gut microbes containing six types of WOR and Tup were shown to assimilate W. Two of the WORs were natively purified and found to contain W. The enzymes catalyzed the conversion of toxic aldehydes to the corresponding acid, with one WOR carrying out an electron bifurcation reaction coupling aldehyde oxidation to the simultaneous reduction of NAD+ and of the redox protein ferredoxin. Such aldehydes are present in cooked foods and are produced as antimicrobials by gut microbiome metabolism. This aldehyde detoxification strategy is dependent on the availability of W to the microbe. The functions of other WORs in the gut microbiome that do not oxidize aldehydes remain unknown. W is generally beyond detection (<6 parts per billion) in common foods and at picomolar concentrations in drinking water, suggesting that W availability could limit some gut microbial functions and might be an overlooked micronutrient.

SUBMITTER: Schut GJ

PROVIDER: S-EPMC8639347 | biostudies-literature | 2021 Oct

REPOSITORIES: biostudies-literature

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Tungsten enzymes play a role in detoxifying food and antimicrobial aldehydes in the human gut microbiome.

Schut Gerrit J GJ Thorgersen Michael P MP Poole Farris L FL Haja Dominik K DK Putumbaka Saisuki S Adams Michael W W MWW

Proceedings of the National Academy of Sciences of the United States of America 20211001 43

Tungsten (W) is a metal that is generally thought to be seldom used in biology. We show here that a W-containing oxidoreductase (WOR) family is diverse and widespread in the microbial world. Surprisingly, WORs, along with the tungstate-specific transporter Tup, are abundant in the human gut microbiome, which contains 24 phylogenetically distinct WOR types. Two model gut microbes containing six types of WOR and Tup were shown to assimilate W. Two of the WORs were natively purified and found to co ...[more]

PMID: 34686601

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Project description:Background: IgA nephropathy (IgAN) is the most common type of glomerulonephritis in Asia. Its pathogenesis involves higher expression of galactose-deficient IgA1 (Gd-IgA1) and dysregulated intestinal mucosal immunity. The objective of this study was to explore whether specific gut microbiota and associated enzymes affect Gd-IgA1 in IgAN. Methods: This study carried out shotgun metagenomic sequencing with Illumina on fecal samples collected from 20 IgAN patients (IgAN group) and 20 healthy controls (HCs group) who were recruited from January 2016 to December 2018 at the Second Clinical College of Guangzhou University of Chinese Medicine. Differences analysis in gut microbiota was performed to determine the overall microbiota composition, the representative enterotypes, and the microbiota abundance. Correlations between gut microbiota and clinical indicators were assessed by Spearman's analysis. Moreover, the functional prediction of microbial communities and the quantitative calculation of enzymes encoded by microbiome were performed using the MetaCyc pathway and the bioBakery three platform, respectively. Results: Bacteroides plebeius and Bacteroides vulgatus levels were higher, while Prevotella copri and Alistipes putredinis levels were lower in the IgAN group compared to HCs group. Enterotype I characterized by Bacteroides was closely related to the IgAN patients. Moreover, Bacteroides fragilis, Flavonifractor plautii and Ruminococcus gnavus were characteristic bacteria enriched in IgAN patients. Spearman's correlation analysis found that Eggerthella lenta and Ruminococcus bromii were positively correlated with urine protein-creatinine ratio, while Ruminococcus gnavus showed a direct association with red blood cells in urine, and Bacteroides vulgatus and Ruminococcus gnavus were positively correlated with eGFR. These results indicated that intestinal dysbacteriosis occurred in IgAN patients and was associated with clinical and biochemical features. In addition, MetaCyc pathway analysis predicted microbiota-related metabolic pathways, including the biosynthesis of amino acids and glycans, were associated with the IgAN group. Microbial enzymes analysis highlighted that Gd-IgA1-associated α-galactosidase and α-N-acetyl-galactosaminidase secreted by Flavonifractor plautii were enriched in IgAN patients. Conclusion: These findings suggested that α-galactosidase and α-N-acetyl-galactosaminidase secreted by Flavonifractor plautii might be related to the production of Gd-IgA1, indicating that enzymes originated from abnormal intestinal microbiota may contribute to the production of Gd-IgA1 and play an important role in the pathogenesis of IgAN.

Dataset Information

Tungsten enzymes play a role in detoxifying food and antimicrobial aldehydes in the human gut microbiome.

Publications

Tungsten enzymes play a role in detoxifying food and antimicrobial aldehydes in the human gut microbiome.

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