The genome of gut microbes encodes a collection of enzymes whose metabolic functions contribute to the bioavailability and bioactivity of unabsorbed (poly)phenols. Datasets from high throughput sequencing, metabolome measurements, and other omics have expanded the understanding of the different modes of actions by which (poly)phenols modulate the microbiome conferring health benefits to the host. Progress have been made to identify direct prebiotic effects of (poly)phenols; albeit up to date, these compounds are not recognized as prebiotics sensu stricto. Interestingly, certain probiotics strains have an enzymatic repertoire, such as tannase, α-L-rhamnosidase, and phenolic acid reductase, involved in the transformation of different (poly)phenols into bioactive phenolic metabolites. In vivo studies have demonstrated that these (poly)phenol-transforming bacteria thrive when provided with phenolic substrates. However, other taxonomically distinct gut symbionts of which a phenolic-metabolizing activity has not been demonstrated are still significantly promoted by (poly)phenols. This is the case of Akkermansia muciniphila, a so-called antiobesity bacterium, which responds positively to (poly)phenols and may be partially responsible for the health benefits formerly attributed to these molecules. We surmise that (poly)phenols broad antimicrobial action free ecological niches occupied by competing bacteria, thereby allowing the bloom of beneficial gut bacteria. This review explores the capacity of (poly)phenols to promote beneficial gut bacteria through their direct and collaborative bacterial utilization and their inhibitory action on potential pathogenic species. We propose the term duplibiotic, to describe an unabsorbed substrate modulating the gut microbiota by both antimicrobial and prebiotic modes of action. (Poly)phenol duplibiotic effect could participate in blunting metabolic disturbance and gut dysbiosis, positioning these compounds as dietary strategies with therapeutic potential.
Extracellular tannase Lactiplantibacillus plantarum-producing strains (TanA+) release bioactive metabolites from dietary tannins. However, there is a paucity of knowledge of TanA+ strains and their hydrolyzing capacities. This study aimed to shed light on the metabolic and genomic features of TanA+ L. plantarum strains and to develop a screening technique. The established spectrophotometric was validated by UPLC-UV-QToF. Eight of 115 screened strains harbored the tanA gene, and six presented TanA activity (PROBI S126, PROBI S204, RKG 1-473, RKG 1-500, RKG 2-219, and RKG 2-690). When cultured with tannic acid (a gallotannin), TanA+ strains released 3.2−11 times more gallic acid than a lacking strain (WCFS1) (p < 0.05). TanA+ strains with gallate decarboxylase (n = 5) transformed this latter metabolite, producing 2.2–4.8 times more pyrogallol than the TanA lacking strain (p < 0.05). However, TanA+ strains could not transform punicalagin (an ellagitannin). Genomic analysis revealed high similarity between TanA+ strains, as only two variable regions of phage and polysaccharide synthesis were distinguished. A phylogenetic analysis of 149 additional genome sequences showed that tanA harboring strains form a cluster and present two bacteriocin coding sequences profile. In conclusion, TanA+ L. plantarum strains are closely related and possess the ability to resist and transform gallotannins. TanA can be screened by the method proposed herein.
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