Tannic Acid-Dependent Modulation of Selected Lactobacillus plantarum Traits Linked to Gastrointestinal Survival

Abstract

BackgroundOwing to its antimicrobial properties dietary tannins may alter the functional efficacy of probiotic lactobacilli in the gastrointestinal (GI)-tract influencing their growth, viability and molecular adaptation to the intestinal environment.Methods and FindingsThe effects of tannic acid on Lactobacillus plantarum WCFS1 were studied by in vitro growth monitoring and visualizing the morphological alteration on the cell wall using transmission electron microscopy. Growth upon tannic acid was characterized by dose-dependent reductions of initial viable counts and extended lag phases. Lag phase-cells growing upon 0.5 mM tannic acid were abnormally shaped and experienced disturbance on the cell wall such as roughness, occasional leakage and release of cell debris, but resumed growth later at tannic acid concentrations high as 2.5 mM. To gain insight on how the response to tannic acid influenced the molecular adaptation of L. plantarum to the GI-tract conditions, gene expression of selected biomarkers for GI-survival was assessed by RT-qPCR on cDNA templates synthetized from mRNA samples obtained from cells treated with 0.5 or 2 mM tannic acid. Tannic acid-dependent gene induction was confirmed for selected genes highly expressed in the gut or with confirmed roles in GI-survival. No differential expression was observed for the pbp2A gene, a biomarker negatively related with GI-survival. However PBP2A was not labeled by Bocillin FL, a fluorescent dye-labeled penicillin V derivative, in the presence of tannic acid which suggests for enhanced GI-survival reportedly associated with the inactivation of this function.ConclusionsProbiotic L. plantarum WCFS1 is able to overcome the toxic effects of tannic acid. This dietary constituent modulates molecular traits linked to the adaptation to intestinal environment in ways previously shown to enhance GI-survival.

Tannin Degradation by a Novel Tannase Enzyme Present in Some Lactobacillus plantarum Strains

“…The presence of the substrate methyl gallate did not affect the expression of tanA Lp ; however, it increased the expression of tanB Lp . This expression behavior allows the assumption that tanB Lp encodes an inducible tannase in L. plantarum ATCC 14917 T , as previously observed in the WCFS1 strain under tannic acid challenge (24).…”

Plant Polyphenols Stimulate Adhesion to Intestinal Mucosa and Induce Proteome Changes in the Probiotic Lactobacillus acidophilus NCFM

“…The glycolytic enzymes pyruvate kinase (PK) and GAPDH both increased in tannic acid‐treated NCFM, indicating elevated ATP production necessary for dealing with environmental stress, as observed in other phenolic‐LAB interactions . By contrast, abundancy of GAPDH was lower when resveratrol or caffeic acid were present during the NCFM culture.…”

Lactobacillus plantarum WCFS1 and its host interaction: a dozen years after the genome

“…Other L. plantarum strains that are suggested to possess tannase‐activity are L. plantarum CNRZ 1228, CNRZ 184, ATCC 8014 and ATCC 14917 (Osawa et al ., ). Culturing of L. plantarum WCFS1 in the presence of tannic acid induces significantly higher expression of persistence and survival genes copA , lp_2940 , ram2 and argG that are highly induced in the GI tract in response to high osmolarity and bile in mice and humans (Reverón et al ., ). L. plantarum WCFS1 is thus able to respond to these toxic compounds as well as use these as an energy source, thereby selectively stimulating its growth.…”

“…On the other hand, tannins have antimicrobial properties; thereby potentially alter the gut composition. L. plantarum is so far the only tannin‐degrading Lactobacillus species found in humans and contains tannase (tannin acyl hydrolase; Reverón et al ., ). L. plantarum WCFS1 is able to hydrolyse tannin into glucose and gallic acid, a harmful and anti‐nutritional compound, which is decarboxylated by LpdB and LpdC ( lp_0271 and lp_2945 ) that encode gallate decarboxylase activity (Jiménez et al ., ).…”