Genetic and biochemical approaches towards unravelling the degradation of gallotannins by Streptococcus gallolyticus
© Jiménez et al.; licensee BioMed Central Ltd. 2014
Received: 30 September 2014
Accepted: 20 October 2014
Published: 31 October 2014
Herbivores have developed mechanisms to overcome adverse effects of dietary tannins through the presence of tannin-resistant bacteria. Tannin degradation is an unusual characteristic among bacteria. Streptococcus gallolyticus is a common tannin-degrader inhabitant of the gut of herbivores where plant tannins are abundant. The biochemical pathway for tannin degradation followed by S. gallolyticus implies the action of tannase and gallate decarboxylase enzymes to produce pyrogallol, as final product. From these proteins, only a tannase (TanBSg) has been characterized so far, remaining still unknown relevant proteins involved in the degradation of tannins.
In addition to TanBSg, genome analysis of S. gallolyticus subsp. gallolyticus strains revealed the presence of an additional protein similar to tannases, TanASg (GALLO_0933). Interestingly, this analysis also indicated that only S. gallolyticus strains belonging to the subspecies “gallolyticus” possessed tannase copies. This observation was confirmed by PCR on representative strains from different subspecies. In S. gallolyticus subsp. gallolyticus the genes encoding gallate decarboxylase are clustered together and close to TanBSg, however, TanASg is not located in the vicinity of other genes involved in tannin metabolism. The expression of the genes enconding gallate decarboxylase and the two tannases was induced upon methyl gallate exposure. As TanBSg has been previously characterized, in this work the tannase activity of TanASg was demonstrated in presence of phenolic acid esters. TanASg showed optimum activity at pH 6.0 and 37°C. As compared to the tannin-degrader Lactobacillus plantarum strains, S. gallolyticus presented several advantages for tannin degradation. Most of the L. plantarum strains possessed only one tannase enzyme (TanBLp), whereas all the S. gallolytcius subsp. gallolyticus strains analyzed possesses both TanASg and TanBSg proteins. More interestingly, upon methyl gallate induction, only the tanB Lp gene was induced from the L. plantarum tannases; in contrast, both tannase genes were highly induced in S. gallolyticus. Finally, both S. gallolyticus tannase proteins presented higher activity than their L. plantarum counterparts.
The specific features showed by S. gallolyticus subsp. gallolyticus in relation to tannin degradation indicated that strains from this subspecies could be considered so far the best bacterial cellular factories for tannin degradation.
KeywordsStreptococcus gallolyticus Tannase Gallate decarboxylase Hydrolase Gallotannins
Tannins are widespread in the plant kingdom, and are often found in woody, lignified tissues . Tannins form weak, pH-dependent and reversible associations with a range of substrates such as cellulose, proteins or enzymes, among others, often making the substrate resistant to microbial attack . Several reports have suggested that the presence of tannins at less than 6% dry matter of the herbivore diet may result in improved animal performance. In contrast, detrimental effects of condensed tannins in excess of 6% dry matter include decreased growth rate and body weight gain, perturbation of mineral absorption, and inhibition of digestive enzymes . Therefore, some herbivores have developed mechanisms to overcome adverse effects of tannins, at least partly, through the presence of tannin-resistant microorganisms .
Streptococcus gallolyticus (formerly known as Streptococcus bovis biotype I) has been isolated as a tannin-resistant bacterium from diverse habitats. It is a normal inhabitant of the rumen and has been isolated from feces of koalas, kangaroos, Japanese large wood mouse, cows, horses, pigs, and guinea pigs -. The presence of S. gallolyticus strains in the digestive tract of herbivores may play an essential role for the host in order to assimilate the tannin-rich diets from their natural habitats. The specific catabolic capacities of S. gallolyticus likely provide this bacterium a selective advantage to survive in the gut of herbivores, where tannins of plant origin are abundant. Therefore, a symbiotic relationship could exist between the animal host and the bacteria to counteract the antinutritional effect of dietary tannins .
S. gallolyticus strains hydrolyzed tannic acid to release gallic acid, which was subsequently decarboxylated to pyrogallol . The proposed biochemical pathway for the degradation of tannins by S. gallolyticus implies the action of a tannase and a gallate decarboxylase enzyme to decarboxylate the gallic acid formed by tannase action . Pyrogallol is formed as a final product from tannin biodegradation . An identical pathway is also used by Lactobacillus plantarum strains to degrade tannins. The L. plantarum genes encoding tannase (tanB Lp , formerly called tanLp1)  and gallate decarboxylase (lpdBCD)  involved in tannin degradation have been identified. In addition, a second tannase gene (tanA Lp ) present in some L. plantarum strains has been recently described . Upon tannin induction, the expression of tanB Lp was induced, whereas tanA Lp expression was not affected . Moreover, TanALp has a specific activity ten times lower than the specific activity calculated for TanBLp tannase.
Similarly to L. plantarum, the genome of S. gallolyticus UCN34 revealed unique features among streptococci related to its adaptation to the rumen environment such as its ability to degrade tannins . Tannins must be degraded by the action of a tannase enzyme . A gene encoding a nonsecreted protein similar to TanBLp (GALLO_1609) was found in the S. gallolyticus UCN34 genome. This protein TanBSg (formerly called TanSg1) has been biochemically characterized recently . In addition, another gene, GALLO_1609, encoding a 596-amino acid long protein 43% identical to the tannase from Staphylococcus lugdunensis (TanASl)  is present in the S. gallolyticus UCN34 genome. From the genes involved in tannin degradation in S. gallolyticus, only the tanB Sg gene encoding a tannase has been identified so far , remaining unknown the genes encoding the gallate decarboxylase enzyme as well as a putative second tannase enzyme. In this work, S. gallolyticus tannase and gallate decarboxylase encoding genes involved in tannin degradation have been identified and their expression comparatively studied. In addition a novel tannase has been characterized. These results provide new relevant insights into S. gallolyticus tannin degradation, a rare biochemical property among bacteria.
Results and discussion
Sequence analysis of S. gallolyticustannase enzymes
The ability to degrade tannins is a specific attribute of S. gallolyticus subsp. gallolyticus deemed important in hostile environments, as tannins are toxic polyphenolic compounds that form strong complexes with proteins and other macromolecules. The S. gallolyticus subsp. gallolyticus UCN34 genome revealed the presence of two proteins similar to tannases, TanASg (GALLO_0933) and TanBSb (GALLO_1609). The tannase proteins from S. lugdunensis (TanASl), L. plantarum (TanALp and TanBLp) and S. gallolyticus (TanASg and TanBSg) were aligned. The alignment revealed that two protein groups could be easily identified. TanA proteins, higher than 60 kDa and possessing a cleavage site of a peptide signal, and TanB proteins, having around 50 kDa of molecular size. The identity degree among TanA and TanB proteins is lower than 30%. The comparison of the amino acid sequence of these tannase proteins with TanBLp, whose tridimensional structure have been recently solved , revealed that the residues important for activity are conserved. All the analyzed proteins possessed the conserved motif Gly-X-Ser-X-Gly typical of serine hydrolases. The catalytic triad identified in the TanBLp structure (Ser-163, Asp-419, and His-451) is only conserved in the TanB proteins. In both TanA proteins Asp-419 is substituted by a Gln residue. This amino acid variation was noticed previously and suggested that the conserved residue Asp-421 may fulfil the role of Asp-419 as the acidic residue of the catalytic triad . The residues identified that make contacts with the three hydroxyl groups of gallic acid (Asp-421, Lys-343, and Glu-357, in TanBLp) are conserved in all the tannase proteins analyzed (Additional file 1: Figure S1A). When TanA proteins were compared identity degrees ranging from 44-50% were found (Additional file 1: Figure S1B). However, the identity among TanB proteins was more lower (32%) (Additional file 1: Figure S1C).
Tannin-induced gene expression of the S. gallolyticusregion involved in tannin degradation
Biochemical properties of S. gallolyticus UCN34 TanASg tannase
When TanBLp was the only tannase described from L. plantarum, homology searched allowed us to identify tanB Sg (GALLO_1609). The gene was cloned and expressed in E. coli, and the recombinant TanBSg protein was biochemically characterized . The data indicated that, as compared to TanBLp, TanBSg possesses remarkable biochemical properties. TanBSg has a specific activity 41% higher than TanBLp, and displays optimum activity at pH 6-8 and 50-70°C, showing high stability over a broad range of temperatures . However, in relation to its substrate range and contrarily to TanBLp, only esters with a short aliphatic alcohol were effectively hydrolyzed by TanBSg. Taking into account only the activity of TanB tannases, it seems that S. gallolyticus could hydrolyze tannins more efficiently than L. plantarum strains.
Different dietary plant varieties produce different types and quantities of phenolic compounds . As the digestive tract of herbivores probably contains different tannins, we focused our studies on the relatively well-define commercially available preparations, tannic acid and epigallocatechin gallate. Tannic acid is almost exclusively formed by poly-galloyl glucose, and gallic acid was observed as the final product of TanASg activity on tannic acid (Figure 6-2). Similarly, gallic acid was released from epigallocatechin as a result of the action of TanASg on epigallocatechin gallate. These results confirmed the capacity of TanASg to degrade dietary tannins.
Once the tannase activity of TanASg was confirmed, their biochemical properties were determined. Since tannase catalyzes the hydrolysis of the galloyl ester linkage releasing gallic acid, the activity of tannase could be measured by estimating the gallic acid formed by the enzyme action . A rhodanine specific method for the detection of gallic acid was used for a reliable quantification of tannase activity . Rhodanine reacts with the vicinal hydroxyl groups of gallic acid to give a red complex with a maximum absorbance at 520 nm. Rhodanine assay was used to determine the specific activity of TanASg. Using methyl gallate as substrate, the specific activity of TanASg was 256 U/mg, 55% or 37% lower than the specific activity of TanBSg (577 U/mg) or TanBLp (408 U/mg); however, it was more than 6 times higher than the activity of the equivalent protein from L. plantarum, TanALp (39 U/mg). These activity data indicated that S. gallolyticus strains have more potential to degrade tannins than L. plantarum strains. These activity data indicated that S. gallolyticus strains have more potential to degrade tannins than L. plantarum strains. Firstly, in L. plantarum only a small number of strains possessed tanA Lp gene, an inducible gene, whereas all the S. gallolytius subsp. gallolyticus strains analyzed so far possesses both tannase genes, being the two genes inducible by gallate esters. More importantly, tannases from S. gallolyticus possess higher specific activity than their counterparts from L. plantarum. A roughly estimation shows that S. gallolyticus strains bearing TanASg and TanBSg posses a two-fold higher tannase activity than most L. plantarum strains possessing only TanBLp tannase.
In addition to TanBSg activity, the biochemical properties showed by TanASg such as high specific activity, optimal temperature (37°C) and broad pH range indicated that S. gallolyticus subsp. gallolyticus strains are so far the bacterial cells better adapted to degrade the tannins present on the diet. It has been described that S. gallolyticus initially responds to tannins with an increased lag phase and decreased growth rate . The response mechanisms used by S. gallolyticus strains enables them to maintain growth and biosynthetic capacity in the presence of high tannin concentrations .
In summary, this study confirmed among bacteria the specific characteristics present in S. gallolyticus subsp. gallolyticus strains which could be important for survival in the gut environment of herbivores, where a large diversity of tannins is present. S. gallolyticus subsp. gallolyticus should be able to degrade these polyphenols and it is known that this bacterium does not depend on other microorganisms for their degradation. The tannin degradation pathway followed by S. gallolyticus subsp. gallolyticus strains implies the combined action of tannase and gallate decarboxylase, which are close on S. gallolyticus genome and seems to act coordinately. In addition, the presence in all the S. gallolyticus subsp. gallolyticus strains of a second, inducible and extracellular tannase enzyme provide them additional advantages for the degradation of high-molecular tannins. The specific features showed by S. gallolyticus subsp. gallolyticus in relation to tannin degradation suggested that these strains are the best bacterial factories for tannin degradation described so far. This explains the widespread occurrence of S. gallolyticus in the rumen of livestock that frequently browse tannin-containing forages, and it is likely that the presence of S. gallolyticus provides a selective advantage to these animals.
Materials and methods
Bacterial strains and growth conditions
S. gallolyticus subsp. gallolyticus UCN34 (CIP 110142) used through this study was kindly provided by Dr. Philippe Glaser (Institut Pasteur, France). S. gallolyticus DSM 13808, S. gallolyticus subsp. gallolyticus DSM 16831T, S. gallolyticus subsp. pasteurianus DSM 15351T, and S. gallolyticus subsp. macedonius DSM 15879T were purchased from the German Collection of Microorganisms and Cell Cultures (DSMZ). Escherichia coli DH10B and E. coli BL21 (DE3) were used as transformation and expression hosts in the pURI3-TEV vector . The S. gallolyticus strains were grown in BHI medium at 37°C without shaking, and the E. coli strains were cultured in Luria-Bertani (LB) medium at 37°C and shaking at 200 rpm.
PCR detection of tannase encoding genes
Genes encoding S. gallolyticus tannases (tanA Sg and tanB Sg ) were amplified by PCR using chromosomal DNA from S. gallolyticus strains. The tanA Sg gene (1.7 kb) was amplified by using primers 803 and 804 (Additional file 3: Table S2). Oligonucleotides 774 and 775 were used to amplify tanB Sg gene (1.4 kb). The reactions were performed in a Personal thermocycler (Eppendorf), using 30°Cycles of denaturation at 94°C for 30 s, annealing at 55°C for 1 min, and extension at 72°C for 2 min. Amplified fragments were resolved in agarose gels.
For RNA isolation, BHI cultures of S. gallolyticus subsp. gallolyticus UCN34 were grown up to an OD 600nm of 1 and then supplemented with methyl gallate at 15 mM final concentration. As control, RNA was also isolated from cultures not supplemented with methyl gallate. The induced cells and their corresponding controls were centrifuged at 4°C after 10 min of exposure to the gallate ester. The pellet was mixed with 2 mL of quenching buffer (60% methanol, 66.7 mM HEPES, pH 6.5, -40°C). Following quenching, the cells were centrifuged at 9,000 × g for 10 min at -10°C and suspended in an extraction mixture (500 μL 1:4 chloroform-acid phenol, 30 μL of 10% SDS, 30 μL Na-acetate 3 M pH 5.2, 400 μL Tris-EDTA buffer [10 mM Tris(hydroxymethyl)amino methane, 1 mM EDTA] pH 7.4, 15 Mg of polyvinylpoly-pyrrolidone, and 500 Mg of glass beads (ϕ, 75-150 μm). The cells were broken under frozen conditions in a Mini-Bead Beater (Biospec Products, INC.) using three treatments of 4600 rpm for 40 seconds and chilled 1 min between cycles. The suspension was then centrifuged at 4°C at 10,000 × g for 2 min. After two extractions with 500 μL of chloroform the supernatant containing the RNA was immediately frozen in liquid nitrogen, and stored at -80°C. NanoDrop ND1000 instrument was used for quantification of RNA. The A260/A280 and A260/A230 ratios were measured to check RNA purity. Integrity and quality of RNA samples were determined by electrophoresis on agarose gels. Two treatments with DNase I (Ambion) were applied and the absence of genomic DNA was confirmed by PCR . The DNA-free RNA was reverse transcribed using the High Capacity cDNA Reverse Transcription Kit (Applied Biosyntems) according to the manufacturer instructions. From the cDNA obtained, quantitative gene expression was analyzed in an AbiPrism 7500 Fast Real Time PCR system (Applied Biosystems). The SYBR Green method was used and each assay was performed in triplicate using SYBR Green real-time PCR Master Mix (Applied Biosystems). Amplification was initiated at 95°C for 10 min, followed by 40°Cycles of 95°C for 15 s and 60°C for 1 min. Control PCRs were included to confirm the absence of primer dimer formation (no-template control), and to verify that there was no DNA contamination (without RT enzyme negative control). Specific primer pairs were designed with the Primer Express 3.0 program to amplify internal regions of tannase and gallate decarboxylase encoding genes (Additional file 3: Table S2). All qPCR assays amplified a single product as determined by melting curve analysis and by electrophoresis. A standard curve was plotted with cycle threshold (Ct) values obtained from amplification of known quantities of cDNA and used to determine the efficiency (E) as E = 10-1/slope. In order to measure S. gallolyticus gene expression, amplification of the endogenous control gene was performed simultaneously and its relative expression compared with that of the target gene. Results were analyzed using the comparative Ct method (also named double delta-delta Ct, 2ΔΔCt method). Genes were considered differentially expressed when a nominal p-values were <0.1 and had a fold change (FC) ≥2. Relative expression levels were calculated with the 7500 Fast System relative quantification software using S. gallolyticus 16S rRNA gene as endogenous gene and the growth in the absence of methyl gallate as growth condition calibrator.
Cloning, expression and purification of TanASg from S. gallolyticus UCN34
The gene encoding a putative tannase (GALLO_0933, or tanA Sg ) in S. gallolyticus UCN34 (accession YP_003430356) was PCR-amplified by PrimeSTAR HS DNA polymerase (Takara). As a peptide signal was predicted in the TanASg sequence, primers 803 and 804 were used to amplify and clone TanASg lacking the 26-amino acid peptide signal sequence. The gene was cloned into the pURI3-TEV vector which encodes expression of a leader sequence containing a six-histidine affinity tag. The purified 1.7-kb PCR product was then inserted into the vector by using a restriction enzyme- and ligation-free cloning strategy .
E. coli DH10B cells were transformed, recombinant plasmids were isolated, and those containing the correct insert were identified by restriction enzyme analysis, verified by DNA sequencing, and then transformed into E. coli BL21 (DE3) cells for expression. E. coli BL21 (DE3) cells carrying the recombinant plasmid, pURI3-TEV-TanASg, were grown at 37°C in LB media containing ampicillin (100 μg/ml) on a rotary shaker (200 rpm) until an optical density at 600 nm of 0.4 was reached. Isopropyl-β-D-thiogalactoside (IPTG) was added to a final concentration of 0.4 mM and protein induction was continued at 22°C for 18 h.
The induced cells were harvested by centrifugation (8,000 g, 15 min, 4°C), resuspended in phosphate buffer (50 mM, pH 6.5) and disrupted by French Press passages (three times at 1,100 psi). The insoluble fraction of the lysate was removed by centrifugation at 47,000 g for 30 min at 4°C. The supernatant was filtered through a 0.2 μm pore-size filter and then applied to a Talon Superflow resin (Clontech) equilibrated in phosphate buffer (50 mM, pH 6.5) containing 3 mM NaCl and 10 mM imidazole to improve the interaction specificity in the affinity chromatography step. The bound enzyme was eluted using 150 mM imidazole in the same buffer. The purity of the enzymes was determined by SDS-PAGE in Tris-glycine buffer. Fractions containing the His6-tagged protein were pooled and analyzed for tannase activity.
Tannase activity assay
Tannase activity was determined using a rhodanine assay specific for gallic acid . Rhodanine reacts only with gallic acid and not with galloyl esters or other phenolics. Gallic acid analysis in the reactions was determined using the following assay. Tannase enzyme (100 μg) in 700 μL of 50 mM phosphate buffer pH 6.5 was incubated with 40 μL of 25 mM methyl gallate (1 mM final concentration) for 5 min at 37°C. After this incubation, 150 μL of a methanolic rhodanine solution (0.667% w/v rhodanine in 100% methanol) were added to the mixture. After 5 min incubation at 30°C, 100 μL of 500 mM KOH was added. After an additional incubation of 5-10 min, the absorbance at 520 nm was measured on a spectrophotometer. A standard curve using gallic acid concentration ranging from 0.125 to 1 mM was prepared. One unit of tannase activity was defined as the amount of enzyme required to release 1 μmol of gallic acid per minute under standard reaction conditions.
Biochemical properties of TanASgtannase
The pH profile of TanASg activity was determined using different 100 mM buffer systems containing acetic acid-sodium acetate (pH 3.0-5.0), citric acid-sodium citrate (pH 6), sodium phosphate (pH 7), Tris-HCl (pH 8), glycine-NaOH (pH 9), and sodium carbonate-bicarbonate (pH 10). The rhodanine assay was used for the optimal pH characterization of tannase. Since the rhodanine-gallic acid complex forms only in basic conditions, after the completion of the enzymatic degradation of methyl gallate, KOH was added to the reaction mixture to ensure that the same pH value (pH 11) was achieved in all samples assayed. Determinations were done in triplicate.
The optimal temperature for purified TanASg tannase was determined in the temperature range 4-65°C in 25 mM phosphate buffer (pH 6.5). For determination of the thermal stability of TanASg, the enzyme in 50 mM phosphate buffer pH 6.5 was preincubated in the absence of substrate at 22, 30, 37, 45, 55 and 65°C for 30 min and 2, 4, 6, and 18 h. Aliquots were withdrawn in triplicate at these incubation times to test the remaining activity under standard conditions. The residual tannase activity was determined at 37°C. The non-heated enzyme was considered as control (100%).
The enzyme was pre-incubated in the presence of various metal salts and chemical agents using final concentrations of 1 mM. The effect of chemical inhibitors and stimulators on TanASg activity was investigated in triplicate by the rhodanine assay using methyl gallate as substrate. The additives analyzed were MgCl2, KCl, CaCl2, HgCl2, ZnCl2, Triton X-100, Urea, Tween 80, EDTA, DMSO, and β-mercaptoethanol. The extent of inhibition or activation of tannase activity was indicated as the percentage of the ratio of residual activity to complete enzyme activity in the control sample without addition of metal ions or chemical agents. Tannase activity measured in the absence of any additive was used as control (100%).
The substrate specificity of TanASg was determined using 17 commercial phenolic esters (methyl gallate, ethyl gallate, propyl gallate, lauryl gallate, methyl benzoate, ethyl benzoate, methyl 4-hydroxybenzoate, ethyl 4-hydroxybenzoate, propyl 4-hydroxybenzoate, butyl 4-hydroxybenzoate, methyl vanillate, methyl 2, 4-dihydroxybenzoate, methyl gentisate, methyl salicylate, ethyl 3, 4-dihydroxybenzoate, ferulic methyl ester, and ferulic ethyl ester) as well as a natural tannins (epigallocatechin gallate, and tannic acid). As controls, phosphate buffer (50 mM, pH 7.0) containing thereagents but lacking the enzyme were incubated in the same conditions.
The hydrolysis products were extracted twice with ethyl acetate (Lab-Scan, Ireland) and analyzed by HPLC-DAD. A Thermo (Thermo Electron Corporation, Waltham, Massachussetts, USA) chromatograph equipped with a P4000 SpectraSystem pump, and AS3000 autosampler, and a UV6000LP photodiode array detector were used. A gradient of solvent A (water/acetic acid, 98:2, v/v) and solvent B (water/acetonitrile/acetic acid, 78:20:2, v/v/v) was applied to a reversed-phase Nova-pack C18 (25°Cm × 4.0 mM i.d.) 4.6 μm particle size, cartridge at room temperature as follows: 0-55 min, 80% B linear, 1.1 mL/min; 55-57 min, 90% B linear, 1.2 mL/min; 57-70 min, 90% B isocratic, 1.2 mL/min; 70-80 min, 95% B linear, 1.2 mL/min; 80-90 min, 100% linear, 1.2 mL/min; 100-120 min, washing 1.0 mL/min, and reequilibration of the column under initial gradient conditions. Detection was performed by scanning from 220 to 380 nm. Samples were injected onto the cartridge after being filtered through a 0.45 μm PVDF filter.
Two-tailed Student’s test performed using GraphPad InStat, version 3.0 (GraphPad Software, San Diego, CA) was used to determine the differences between means. The data are representative means of at least three independent experiments.
NJ, IR and MET performed the experiments and drafted the manuscript. FLF, BR and RM participated in the design of the study and supervised the study. All authors revised and approved the final manuscript.
This work was financially supported by grants AGL2011-22745, S2009/AGR-1469 (ALIBIRD) (Comunidad de Madrid), and RM2012-00004 (INIA). We acknowledge support of the publication fee by the CSIC Open Access Publication Support Initiative through its Unit of Information Resources for Research (URICI). We are grateful to J. M. Barcenilla and M. V. SantaMaría for their assistance. N. Jiménez is a recipient of a FPI fellowship from the MINECO and M. Esteban-Torres is a recipient of a JAE predoctoral fellowship from the CSIC.
- Serrano J, Puupponen-Pimiä R, Dauer A, Aura A-M, Saura-Calixto F: Tannins: current knowledge of food sources, intake, bioavailability and biological effects. Mol Nutr Food Res. 2009, 53: S310-S329. 10.1002/mnfr.200900039.View ArticleGoogle Scholar
- Mingshu L, Kai Y, Quiang H, Dongying J: Biodegradation of gallotannins and ellagitannins. J Basic Microbiol. 2006, 46: 68-84. 10.1002/jobm.200510600.View ArticleGoogle Scholar
- Barry TN, Manley TR: Interrelationships between the concentrations of total condensed tannin, free condensed tannin and lignin in Lotus sp. and their possible consequences in ruminant nutrition. J Sci Food Agric. 1986, 37: 248-254. 10.1002/jsfa.2740370309.View ArticleGoogle Scholar
- Krause DO, Smith WJM, Broker JD, McSweeney CS: Tolerance mechanisms of streptococci to hydrolysable and condensed tannins. Anim Feed Sci Tech. 2005, 121: 59-75. 10.1016/j.anifeedsci.2005.02.008.View ArticleGoogle Scholar
- Osawa R, Fujisawa T, Sly LI: Streptococcus gallolyticus sp. nov.; gallate degrading organisms formerly assigned to Streptococcus bovis. System Appl Microbiol. 1995, 18: 74-78. 10.1016/S0723-2020(11)80451-0.View ArticleGoogle Scholar
- Sly LI, Cahill M, Osawa R, Fujisawa T: The tannin-degrading species Streptococcus gallolyticus and Streptococcus caprinus are subjective synonyms. Int J Syst Bacteriol. 1997, 47: 893-894. 10.1099/00207713-47-3-893.View ArticleGoogle Scholar
- Sasaki E, Shimada T, Osawa R, Nishitani Y, Spring S, Lang E: Isolation of tannin-degrading bacteria isolated from feces of the Japanese large wood mouse, Apodemus speciosus, feeding on tannin-rich acorns. Syst Appl Microbiol. 2005, 28: 358-365. 10.1016/j.syapm.2005.01.005.View ArticleGoogle Scholar
- Chamkha M, Patel BKC, Traore A, Garcia JL, Labat M: Isolation from a shea cake digester of a tannin-degrading Streptococcus gallolyticus strain that decarboxylates protocatechuic acid hydroxycinnamic acids, and emendation of the species. Int J System Evol Microbiol. 2002, 52: 939-944. 10.1099/ijs.0.01909-0.Google Scholar
- Iwamoto K, Tsuruta H, Nishitaini Y, Osawa R: Identification and cloning of a gene encoding tannase (tannin acylhydrolase) fromLactobacillus plantarumATCC 14917T.Syst Appl Microbiol 2008, 31:269–277.,Google Scholar
- Jiménez N, Curiel JA, Reverón I, de las Rivas B, Muñoz R: Uncovering the Lactobacillus plantarum WCFS1 gallate decarboxylase involved in tannin degradation. Appl Environ Microbiol. 2013, 79: 4253-4263. 10.1128/AEM.00840-13.View ArticleGoogle Scholar
- Jiménez N, Esteban-Torres M, Mancheño JM, de las Rivas B, Muñoz R: Tannin degradation by a second tannase enzyme present in some Lactobacillus plantarum strains. Appl Environ Microbiol. 2014, 80: 2991-2997. 10.1128/AEM.00324-14.View ArticleGoogle Scholar
- Rusniok C, Couvé E, da Cunha V, El Gana R, Zidane N, Bouchier C, Poyart C, Leclercq R, Trieu-Cuot P, Glaser P: Genome sequence of Streptococcus gallolyticus: insights into its adaptation to the bovine rumen and its ability to cause endocarditis. J Bacteriol. 2010, 192: 2266-2276. 10.1128/JB.01659-09.View ArticleGoogle Scholar
- Chávez-González M, Rodríguez-Durán LV, Balagurusamy N, Prado-Barragán A, Rodríguez R, Contreras JC, Aguilar CN: Biotechnological advances and challenges of tannase: an overview. Food Bioprocess Technol. 2012, 5: 445-459. 10.1007/s11947-011-0608-5.View ArticleGoogle Scholar
- Jiménez N, Barcenilla JM, López de Felipe F, de las Rivas B, Muñoz R: Characterization of a bacterial tannase from Streptococcus gallolyticus UCN34 suitable for tannin biodegradation. Appl Microbiol Biotechnol. 2014, 98: 6329-6337. 10.1007/s00253-013-5253-7.View ArticleGoogle Scholar
- Noguchi N, Ohashi T, Shiratori T, Narui K, Hagiwara T, Ko M, Watanabe K, Miyahara T, Taira S, Moriyasu F, Sasatsu M: Association of tannase-producing Staphylococcus lugdunensis with colon cancer and characterization of a novel tannase gene. J Gastroenterol. 2007, 42: 346-351. 10.1007/s00535-007-2012-5.View ArticleGoogle Scholar
- Schlegel L, Grimont F, Ageron E, Grimont PAD, Bouvet A: Reappraisal of the taxonomy of the Streptococcus bovis/Streptococcus equinus complex and related species: description of Streptococcus gallolyticus subsp. gallolyticus subsp. nov., S. gallolyticus subsp. macedonius subsp. nov. and S. gallolyticus subsps. pasteurianus subsp. nov. Int J System Evol Microbiol. 2003, 53: 631-645. 10.1099/ijs.0.02361-0.View ArticleGoogle Scholar
- Ren B, Wu M, Wang Q, Peng X, Wen H, McKinstry WJ, Chen Q: Crystal structure of tannase from Lactobacillus plantarum. J Mol Biol. 2013, 425: 2737-2751. 10.1016/j.jmb.2013.04.032.View ArticleGoogle Scholar
- Curiel JA, Rodríguez H, Acebrón I, Mancheño JM, de las Rivas B, Muñoz R: Production and physicochemical properties of recombinant Lactobacillus plantarum tannase. J Agric Food Chem. 2009, 57: 6224-6230. 10.1021/jf901045s.View ArticleGoogle Scholar
- Hakkinen SH, Torronen AR: Content of flavonols and selected phenolic acids in strawberries and Vaccinium species: Influence of cultivar, cultivation site and technique. Food Res Int. 2000, 33: 517-524. 10.1016/S0963-9969(00)00086-7.View ArticleGoogle Scholar
- Mueller-Harvey I: Analysis of hydrolysable tannins. Animal Feed Sci Technol. 2001, 91: 3-20. 10.1016/S0377-8401(01)00227-9.View ArticleGoogle Scholar
- Inoue KH, Hagerman AE: Determination of gallotannins with rhodanine. Anal Biochem. 1988, 169: 363-369. 10.1016/0003-2697(88)90296-5.View ArticleGoogle Scholar
- O’Donovan L, Brooker JD: Effect of hydrolysable and condensed tannins on growth, morphology and metabolism of Streptococcus gallolyticus (S. caprinus) and Streptococcus bovis. Microbiology. 2001, 147: 1025-1033.View ArticleGoogle Scholar
- Curiel JA, de las Rivas B, Mancheño JM, Muñoz R: The pURI family of expression vectors: a versatile set of ligation independent cloning plasmids for producing recombinant His-fusion proteins. Prot Expr Purif. 2011, 76: 44-53. 10.1016/j.pep.2010.10.013.View ArticleGoogle Scholar
- Saulnier DM, Molenaar D, de Vos WM, Gibson GR, Kolida S: Identification of prebiotic fructooligosaccharide metabolism in Lactobacillus plantarum WCFS1 through microarrays. Appl Environ Microbiol. 2007, 73: 1753-1765. 10.1128/AEM.01151-06.View ArticleGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.