Abstract
BackgroundGallic acid (GA) is a model hydroxybenzoic acid that occurs esterified in the lignocellulosic biomass of higher plants. GA displays relevant biological activities including anticancer properties. Owing to its antimicrobial and cellulase-inhibiting activities, GA also imposes constraints to the fermentability of lignocellulosic hydrolysates. In depth-knowledge of the mechanisms used by tolerant microorganisms to adapt to hydroxybenzoic acids would be a step forward to improve the bioavailability of GA or select/engineer production hosts with improved metabolic traits for the bioconversion of pretreated lignocellulosic biomass.ResultsWhole genome transcriptional profiling using DNA microarrays was used to characterize the molecular response of Lactobacillus plantarum WCFS1 to GA. Expression levels of 14 and 40 genes were differentially regulated at 1.5 and 15 mM GA, respectively. The transcriptomic analysis identified a marked induction of genes with confirmed or related roles to gastrointestinal survival, the repression of genes coding for certain ABC-type transporters and modulation of genes involved in the control of intracellular ammonia levels, among other responses. Most notably, a core set of genes dedicated to produce GA from polyphenols (tanBLp), decarboxylate GA to pyrogallol (lpdB, lpdC and lpdD) and transport functions (lp_2943) was highly overexpressed at both GA concentrations. Correspondingly, resting cells of strain WCFS1 induced by GA, but not their non-induced controls, produced pyrogallol. Gene expression and organization of genes involved in GA metabolism suggested a chemiosmotic mechanism of energy generation. Resting cells of L. plantarum induced by GA generated a membrane potential and a pH gradient across the membrane immediately upon addition of GA. Altogether, transcriptome profiling correlated with physiological observations indicating that a proton motive force could be generated during GA metabolism as a result of electrogenic GA uptake coupled with proton consumption by the intracellular gallate decarboxylase.ConclusionsThe combination of transcriptome and physiological analyses revealed versatile molecular mechanisms involved in the adaptation of L. plantarum to GA. These data provide a platform to improve the survival of Lactobacillus in the gut. Our data may also guide the selection/engineering of microorganisms that better tolerate phenolic inhibitors present in pretreated lignocellulosic feedstocks.Electronic supplementary materialThe online version of this article (doi:10.1186/s12934-015-0345-y) contains supplementary material, which is available to authorized users.
Highlights
Gallic acid (GA) is a model hydroxybenzoic acid that occurs esterified in the lignocellulosic biomass of higher plants
Global transcriptomic responses during adaptation to GA To investigate the adaptive response of L. plantarum WCFS1 to GA, the transcriptomic profile of L. plantarum WCFS1 was defined in cells exponentially growing in medium devoid of GA after 10 min of exposure to 1.5 or 15 mM of this compound
The transcriptome signature of GA response coincided with physiological analyses to show that the GA catabolic pathway required induction by the substrate (GA), and that the energetic consequence of GA metabolism in L. plantarum was the generation of a proton motive force (PMF)
Summary
Gallic acid (GA) is a model hydroxybenzoic acid that occurs esterified in the lignocellulosic biomass of higher plants. GA displays relevant biological activities including anticancer properties. Edible plants are the main sources of dietary phenolic acids, hydroxycinnamic and hydroxybenzoic acids, which are micronutrients with significant biological properties. GA displays relevant biological activities including anti-inflammatory [2] or antiviral ones [3] and has attracted interest because of its reported anticancer properties in animal and in vitro studies (reviewed in [4]). A better understanding of the tolerance of gut microbiota to these health-relevant compounds will be a step forward to improve the persistence of beneficial microorganisms in the intestine
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