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      Gut Bacteria Involved in Ellagic Acid Metabolism To Yield Human Urolithin Metabotypes Revealed

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          Abstract

          We aimed to elucidate the gut bacteria that characterize the human urolithin metabotypes A and B (UM-A and UM-B). We report here a new bacterium isolated from the feces of a healthy woman, capable of producing the final metabolites urolithins A and B and different intermediates. Besides, we describe two gut bacterial co-cultures that reproduced the urolithin formation pathways upon in vitro fermentation of both UM-A and UM-B. This is the first time that the capacity of pure strains to metabolize ellagic acid cooperatively to yield urolithin profiles associated with UM-A and UM-B has been demonstrated. The urolithin-producing bacteria described herein could have potential as novel probiotics and in the industrial manufacture of bioactive urolithins to develop new ingredients, beverages, nutraceuticals, pharmaceuticals, and (or) functional foods. This is especially relevant in UM-0 individuals since they cannot produce bioactive urolithins.

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          Ellagic acid metabolism by human gut microbiota: consistent observation of three urolithin phenotypes in intervention trials, independent of food source, age, and health status.

          Francisco Tomás-Barberán, Rocío García-Villalba, Antonio González-Sarrías … (2014)
          Three phenotypes for urolithin production after ellagitannin and ellagic acid intake are consistently observed in different human intervention trials. Subjects can be stratified into three urolithin-producing groups. "Phenotype A" produced only urolithin A conjugates, which included between 25 and 80% of the volunteers in the different trials. "Phenotype B" produced isourolithin A and/or urolithin B in addition to urolithin A, this being the second relevant group (10-50%). "Phenotype 0" (5-25%) was that in which these urolithins were not detected. The three phenotypes were observed independently of the volunteers' health status and demographic characteristics (age, gender, body mass index (BMI)) and of the amount or type of ellagitannin food source ingested (walnuts and other nuts, strawberries, raspberries, and other berries or pomegranates). Interestingly, a higher percentage of phenotype B was observed in those volunteers with chronic illness (metabolic syndrome or colorectal cancer) associated with gut microbial imbalance (dysbiosis). These urolithin phenotypes could show differences in the human gut microbiota and should be considered in intervention trials dealing with health benefits of ellagitannins or ellagic acid. Whether this phenotypic variation could be a biomarker related to differential health benefits or illness predisposition deserves further research.
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            Description of urolithin production capacity from ellagic acid of two human intestinal Gordonibacter species.

            María V Selma, David Beltran, Rocío García-Villalba … (2014)
            Ellagitannin and ellagic acid metabolism to urolithins in the gut shows a large human interindividual variability and this has been associated with differences in the colon microbiota. In the present study we describe the isolation of one urolithin-producing strain from the human faeces of a healthy volunteer and the ellagic acid transformation to different urolithin metabolites by two species of intestinal bacteria. The isolate belongs to a new species described as Gordonibacter urolithinfaciens, sp. nov. The type strain of the Gordonibacter genus, Gordonibacter pamelaeae DSM 19378(T), was also demonstrated to produce urolithins. Both human intestinal bacteria grew similarly in the presence and absence of ellagic acid at 30 μM concentration. Ellagic acid catabolism and urolithin formation occurred during the stationary phase of the growth of the bacteria under anaerobic conditions. The HPLC-MS analyses showed the sequential production of pentahydroxy-urolithin (urolithin M-5), tetrahydroxy-urolithin (urolithin M-6) and trihydroxy-urolithin (urolithin C), while dihydroxy-urolithins (urolithin A and isourolithin A), and monohydroxy-urolithin (urolithin B) were not produced in pure cultures. Consequently, either other bacteria from the gut or the physiological conditions found in vivo are necessary for completing metabolism until the final urolithins (dihydroxy and monohydroxy urolithins) are produced. This is the first time that the urolithin production capacity of pure strains has been demonstrated. The identification of the urolithin-producing bacteria is a relevant outcome as urolithin implication in health (cardiovascular protection, anti-inflammatory and anticarcinogenic properties) has been supported by different bioassays and urolithins can be used in the development of functional foods and nutraceuticals. This study represents an initial work that opens interesting possibilities of describing enzymatic activities involved in urolithin production that can help in understanding both the human interindividual differences in polyphenol metabolism, the microbial pathways involved, and the role of polyphenols in human health. The presence of urolithin producing bacteria can indirectly affect the health benefits of ellagitannin consumption.
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              Urolithins, the rescue of "old" metabolites to understand a "new" concept: Metabotypes as a nexus among phenolic metabolism, microbiota dysbiosis, and host health status.

              Francisco Tomás-Barberán, Antonio González-Sarrías, Rocío García-Villalba … (2017)
              Urolithins are dibenzo[b,d]pyran-6-one derivatives that are produced by the human gut microbiota from ellagitannins and ellagic acid (EA). These metabolites are much better absorbed than their precursors and have been suggested to be responsible for the health effects attributed to ellagitannins and EA that occur in food products as berries and nuts. In the present review, the role and potential of urolithins in human health are critically reviewed, and a perspective of the research approach needed to demonstrate these health effects is presented, based on the existing knowledge. The analytical methods available for urolithin analysis, their occurrence in different tissues and biological fluids, and their metabolism by human gut microbiota are considered. In addition, the interindividual variability observed for the production of urolithins (metabotypes) and its relationship with health status and dysbiosis are also reviewed. The potential mechanisms of action of urolithins are also critically discussed, paying attention to the concentration and the type of metabolites used in the in vitro and in vivo assays and the physiological significance of the results obtained. The gut microbiota metabolism of EA to urolithins and that of daidzein to equol, their individual variations, and the effects on health are also compared.
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                Author and article information

                Journal
                Journal ID (nlm-ta): J Agric Food Chem
                Journal ID (iso-abbrev): J Agric Food Chem
                Journal ID (publisher-id): jf
                Journal ID (coden): jafcau
                Title: Journal of Agricultural and Food Chemistry
                Publisher: American Chemical Society
                ISSN (Print): 0021-8561
                ISSN (Electronic): 1520-5118
                Publication date (Electronic): 25 February 2023
                Publication date Collection: 08 March 2023
                Volume: 71
                Issue: 9
                Pages: 4029-4035
                Affiliations
                [1]Laboratory of Food & Health, Research Group on Quality, Safety, and Bioactivity of Plant Foods, CEBAS-CSIC , Murcia 30100, Spain
                Author notes
                [* ]Email: mvselma@ 123456cebas.csic.es . Fax: +34-968-396213.
                Author information
                https://orcid.org/0000-0003-1883-1673
                https://orcid.org/0000-0002-1068-8692
                https://orcid.org/0000-0002-0790-1739
                https://orcid.org/0000-0002-6780-974X
                Article
                DOI: 10.1021/acs.jafc.2c08889
                PMC ID: 9999415
                PubMed ID: 36840624
                SO-VID: 9cbabace-91e0-4954-a76a-362523a136fa
                Copyright © © 2023 The Authors. Published by American Chemical Society
                License:

                Permits the broadest form of re-use including for commercial purposes, provided that author attribution and integrity are maintained ( https://creativecommons.org/licenses/by/4.0/).

                History
                Date received : 16 December 2022
                Date accepted : 09 February 2023
                Date revision received : 30 January 2023
                Funding
                Funded by: Fundación Séneca, doi 10.13039/100007801;
                Award ID: 20880/PI/18
                Funded by: Neuroaging PTI+ platform, doi NA;
                Award ID: NA
                Funded by: Ministerio de Ciencia e Innovación, doi 10.13039/501100004837;
                Award ID: PID2019-103914RB-I00
                Funded by: Ministerio de Ciencia e Innovación, doi 10.13039/501100004837;
                Award ID: FPU18/03961
                Funded by: Ministerio de Ciencia e Innovación, doi 10.13039/501100004837;
                Award ID: AEI /10.13039/501100011033
                Funded by: Consejo Superior de Investigaciones Científicas, doi 10.13039/501100003339;
                Award ID: PIE 202270E057
                Funded by: Fundación Séneca, doi 10.13039/100007801;
                Award ID: 21647/PDC/21
                Categories
                Subject: Article
                Custom metadata
                document-id-old-9 jf2c08889
                document-id-new-14 jf2c08889
                ccc-price

                ScienceOpen disciplines: Food science & Technology
                Keywords: polyphenols,metabolism,gut microbiota,interindividual variability,urolithin-producing bacteria
                Data availability:
                ScienceOpen disciplines: Food science & Technology
                Keywords: polyphenols, metabolism, gut microbiota, interindividual variability, urolithin-producing bacteria

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