Genetic and biochemical approaches towards unravelling the degradation of gallotannins by Streptococcus gallolyticus

Jiménez, Natalia; Reverón, Inés; Esteban-Torres, María; Felipe, Félix López de; Rivas, Blanca de las; Múñoz, Rosario

doi:10.1186/s12934-014-0154-8

Cited by 18 publications

(23 citation statements)

References 24 publications

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“…In relation to tannase substrates, it has been described that only the esters derived from gallic and protocatechuic acids were hydrolyzed (5,6,39,40,43). It seems that other hydroxybenzoic acids without hydroxyl groups and with substituents other than OH or OOH at position 2 are not metabolized by bacterial tannases.…”

Section: Methodsmentioning

confidence: 99%

“…3B). Surprisingly, Est_1092 also exhibited activity against the two model hydroxybenzoic esters hydrolyzed by bacterial tannases (tannin acyl hydrolases), gallate and protocatechuate esters (5,6,39,40). The specific activity of Est_1092 on methyl gallate hydrolysis was compared to the activity reported for the two tannase enzymes (TanA Lp and TanB Lp ) previously described on L. plantarum (6).…”

Section: Methodsmentioning

confidence: 99%

“…The buffers (100 mM) used were acetic acid-sodium acetate (pH 3 to 5), sodium phosphate (pH 6 to 7), Tris-HCl (pH 8), and glycine-NaOH (pH 9). The optimal temperature was assayed by incubating purified Est_1092 esterase in 50 mM McIlvaine buffer (pH 5.0) at different temperatures (5,20,30,37,40,45,55, and 65°C). For temperature stability measurements, the recombinant esterase was incubated in 50 mM McIlvaine buffer, pH 5.0, at 20, 30, 37, 45, 55, and 65°C for 5, 15, and 30 min and 1, 2, 4, 6, and 20 h. Aliquots were withdrawn at these incubation times to test the remaining activity under standard conditions.…”

Section: Methodsmentioning

confidence: 99%

See 2 more Smart Citations

A Lactobacillus plantarum Esterase Active on a Broad Range of Phenolic Esters

Esteban-Torres

Landete

Reverón

et al. 2015

Appl Environ Microbiol

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bLactobacillus plantarum is the lactic acid bacterial species most frequently found in the fermentation of food products of plant origin on which phenolic compounds are abundant. L. plantarum strains showed great flexibility in their ability to adapt to different environments and growth substrates. Of 28 L. plantarum strains analyzed, only cultures from 7 strains were able to hydrolyze hydroxycinnamic esters, such as methyl ferulate or methyl caffeate. As revealed by PCR, only these seven strains possessed the est_1092 gene. When the est_1092 gene was introduced into L. plantarum WCFS1 or L. lactis MG1363, their cultures acquired the ability to degrade hydroxycinnamic esters. These results support the suggestion that Est_1092 is the enzyme responsible for the degradation of hydroxycinnamic esters on the L. plantarum strains analyzed. The Est_1092 protein was recombinantly produced and biochemically characterized. Surprisingly, Est_1092 was able to hydrolyze not only hydroxycinnamic esters, since all the phenolic esters assayed were hydrolyzed. Quantitative PCR experiments revealed that the expression of est_1092 was induced in the presence of methyl ferulate, an hydroxycinnamic ester, but was inhibited on methyl gallate, an hydroxybenzoic ester. As Est_1092 is an enzyme active on a broad range of phenolic esters, simultaneously possessing feruloyl esterase and tannase activities, its presence on some L. plantarum strains provides them with additional advantages to survive and grow on plant environments. Lactobacillus plantarum is a highly versatile lactic acid bacterial species found in many different ecological niches, such as vegetables, meat, fish, and dairy products, as well as in the gastrointestinal tract (1). The genome of L. plantarum strain WCFS1 was the first to be fully sequenced, and it was, in fact, the first of any of the Lactobacillus genomes to be published (2). When the genome diversity of L. plantarum on a full genome scale was analyzed, it was revealed that L. plantarum strains are predicted to lack 9 to 20% of the genes of the L. plantarum WCFS1 reference genome, and about 50 genes appeared to be specific to strain WCFS1, as they were not found in any other strain (1). This variability confirms the flexibility of L. plantarum in its ability to adapt to different environments and growth substrates.Phenolic compounds are important constituents of food products of plant origin, as they are related to the sensory characteristics of the food and are beneficial to consumer health (3). Therefore, it is interesting to know the metabolic pathways of biosynthesis or degradation of these compounds in bacteria. L. plantarum is the lactic acid bacterium that is the most frequently found in the fermentation of food products of plant origin, being the bacterial model for the study of phenolic compound metabolism (4). Among these compounds, the metabolism of phenolic esters is greatly relevant, as they are widely spread throughout the plant kingdom (3). Esters of phenolic acids mainly belong to two distingui...

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Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

See 1 more Smart Citation

A Lactobacillus plantarum Esterase Active on a Broad Range of Phenolic Esters

Esteban-Torres

Landete

Reverón

et al. 2015

Appl Environ Microbiol

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“…Apart from Streptococcus gallolyticus (3,4), species of the L. plantarum group are the only lactic acid bacteria that possess tannase activity (5,6). The biochemical pathway used by L. plantarum to hydrolyze tannic acid produces gallic acid and glucose, and the gallic acid formed is subsequently decarboxylated to pyrogallol (7).…”

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confidence: 99%

Differential Gene Expression by Lactobacillus plantarum WCFS1 in Response to Phenolic Compounds Reveals New Genes Involved in Tannin Degradation

Reverón

Jiménez

Curiel

et al. 2017

Appl Environ Microbiol

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Lactobacillus plantarum is a lactic acid bacterium that can degrade food tannins by the successive action of tannase and gallate decarboxylase enzymes. In the L. plantarum genome, the gene encoding the catalytic subunit of gallate decarboxylase (lpdC, or lp_2945) is only 6.5 kb distant from the gene encoding inducible tannase (L. plantarum tanB [tanB Lp ], or lp_2956). This genomic context suggests concomitant activity and regulation of both enzymatic activities. Reverse transcription analysis revealed that subunits B (lpdB, or lp_0271) and D (lpdD, or lp_0272) of the gallate decarboxylase are cotranscribed, whereas subunit C (lpdC, or lp_2945) is cotranscribed with a gene encoding a transport protein (gacP, or lp_2943). In contrast, the tannase gene is transcribed as a monocistronic mRNA. Investigation of knockout mutations of genes located in this chromosomal region indicated that only mutants of the gallate decarboxylase (subunits B and C), tannase, GacP transport protein, and TanR transcriptional regulator (lp_2942) genes exhibited altered tannin metabolism. The expression profile of genes involved in tannin metabolism was also analyzed in these mutants in the presence of methyl gallate and gallic acid. It is noteworthy that inactivation of tanR suppresses the induction of all genes overexpressed in the presence of methyl gallate and gallic acid. This transcriptional regulator was also induced in the presence of other phenolic compounds, such as kaempferol and myricetin. This study complements the catalog of L. plantarum expression profiles responsive to phenolic compounds, which enable this bacterium to adapt to a plant food environment.IMPORTANCE Lactobacillus plantarum is a bacterial species frequently found in the fermentation of vegetables when tannins are present. L. plantarum strains degrade tannins to the less-toxic pyrogallol by the successive action of tannase and gallate decarboxylase enzymes. The genes encoding these enzymes are located close to each other in the chromosome, suggesting concomitant regulation. Proteins involved in tannin metabolism and regulation, such GacP (gallic acid permease) and TanR (tannin transcriptional regulator), were identified by differential gene expression in knockout mutants with mutations in genes from this region. This study provides insights into the highly coordinated mechanisms that enable L. plantarum to adapt to plant food fermentations.

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“…Gallic acid will be decarboxylated by a gallate decarboxylase to pyrogallol (PG) 23 . Of note, Jiménez et al considered Sgg as the best bacterial cellular factories for (gallo)tannin degradation so far known 24 .…”

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Streptococcus gallolyticus abrogates anti-carcinogenic properties of tannic acid on low-passage colorectal carcinomas

Oehmcke-Hecht

Mandl

Naatz

et al. 2020

Sci Rep

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the tannase-producing Gram-positive bacterial species Streptococcus gallolyticus subsp. gallolyticus (Sgg) is an opportunistic pathogen of the human gut and strongly associated with colorectal cancer (cRc). A unique feature of Sgg is its ability to degrade tannic acids (tA). tA constitute an important part of the human diet with known anti-tumorigenic properties. Here, we examined whether Sgg is able to protect tumor cells from the toxic effect of TA and thus drive tumorigenesis indirectly. Human CRC cell lines (n = 8) were treated with increasing concentrations of TA. We confirmed the cytotoxic activity of TA in a dose-dependent manner. In virtually all cell lines, viability decreased significantly (>60% inhibition). Moreover, pyrogallol, the degradation product of TA, had no effect on the tested cell lines. This suggests a specific effect of TA. Cytotoxicity was due to necrosis and induction of senescence in residual cells. finally, when tA was degraded by Sgg, the cytotoxic effect could be abolished. Tumor cells even responded with boosted cell proliferation, highlighting the impact of Sgg on cRc progression. We here provide another piece of evidence for the active interplay between Sgg and cancer preventive components. these data will help to move forward in designing concepts for therapeutic and eventually also prophylactic approaches to combat gastrointestinal malignancies.

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Genetic and biochemical approaches towards unravelling the degradation of gallotannins by Streptococcus gallolyticus

Cited by 18 publications

References 24 publications

A Lactobacillus plantarum Esterase Active on a Broad Range of Phenolic Esters

A Lactobacillus plantarum Esterase Active on a Broad Range of Phenolic Esters

Differential Gene Expression by Lactobacillus plantarum WCFS1 in Response to Phenolic Compounds Reveals New Genes Involved in Tannin Degradation

Streptococcus gallolyticus abrogates anti-carcinogenic properties of tannic acid on low-passage colorectal carcinomas

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