scholarly journals Enzymes Catalyzing the TCA- and Urea Cycle Influence the Matrix Composition of Biofilms Formed by Methicillin-Resistant Staphylococcus aureus USA300

2018 ◽  
Vol 6 (4) ◽  
pp. 113 ◽  
Author(s):  
Sarah De Backer ◽  
Julia Sabirova ◽  
Ines De Pauw ◽  
Henri De Greve ◽  
Jean-Pierre Hernalsteens ◽  
...  
Keyword(s):  
Staphylococcus Aureus ◽  
Urea Cycle ◽  
Citrate Synthase ◽  
Fumarate Hydratase ◽  
Tca Cycle ◽  
Matrix Composition ◽  
Methicillin Resistant ◽  
The Tca Cycle ◽  
The Matrix ◽  
Biofilm Matrix

In methicillin-sensitive Staphylococcus aureus (MSSA), the tricarboxylic acid (TCA) cycle is known to negatively regulate production of the major biofilm-matrix exopolysaccharide, PIA/PNAG. However, methicillin-resistant S. aureus (MRSA) produce a primarily proteinaceous biofilm matrix, and contribution of the TCA-cycle therein remains unclear. Utilizing USA300-JE2 Tn-mutants (NARSA) in genes encoding TCA- and urea cycle enzymes for transduction into a prolific biofilm-forming USA300 strain (UAS391-Erys), we studied the contribution of the TCA- and urea cycle and of proteins, eDNA and PIA/PNAG, to the matrix. Genes targeted in the urea cycle encoded argininosuccinate lyase and arginase (argH::Tn and rocF::Tn), and in the TCA-cycle encoded succinyl-CoA synthetase, succinate dehydrogenase, aconitase, isocitrate dehydrogenase, fumarate hydratase class II, and citrate synthase II (sucC::Tn, sdhA/B::Tn, acnA::Tn, icd::Tn, fumC::Tn and gltA::Tn). Biofilm formation was significantly decreased under no flow and flow conditions by argH::Tn, fumC::Tn, and sdhA/B::Tn (range OD492 0.374−0.667; integrated densities 2.065−4.875) compared to UAS391-EryS (OD492 0.814; integrated density 10.676) (p ≤ 0.008). Cellular and matrix stains, enzymatic treatment (Proteinase K, DNase I), and reverse-transcriptase PCR-based gene-expression analysis of fibronectin-binding proteins (fnbA/B) and the staphylococcal accessory regulator (sarA) on pre-formed UAS391-Erys and Tn-mutant biofilms showed: (i) < 1% PIA/PNAG in the proteinaceous/eDNA matrix; (ii) increased proteins under no flow and flow in the matrix of Tn mutant biofilms (on average 50 and 51 (±11)%) compared to UAS391-Erys (on average 22 and 25 (±4)%) (p < 0.001); and (iii) down- and up-regulation of fnbA/B and sarA, respectively, in Tn-mutants compared to UAS391-EryS (0.62-, 0.57-, and 2.23-fold on average). In conclusion, we show that the biofilm matrix of MRSA-USA300 and the corresponding Tn mutants is PIA/PNAG-independent and are mainly composed of proteins and eDNA. The primary impact of TCA-cycle inactivation was on the protein component of the biofilm matrix of MRSA-USA300.

scholarly journals The existence of a nonclassical TCA cycle in the nucleus that wires the metabolic-epigenetic circuitry

2021 ◽  
Vol 6 (1) ◽  
Author(s):  
Xujun Liu ◽  
Wenzhe Si ◽  
Lin He ◽  
Jianguo Yang ◽  
Yani Peng ◽  
...  
Keyword(s):  
Epigenetic Regulation ◽  
Citrate Synthase ◽  
Fumarate Hydratase ◽  
Tca Cycle ◽  
Chromatin Dynamics ◽  
Metabolic Intermediates ◽  
The Tca Cycle ◽  
Transport Chain ◽  
Outstanding Question ◽  
Aconitase 2

AbstractThe scope and variety of the metabolic intermediates from the mitochondrial tricarboxylic acid (TCA) cycle that are engaged in epigenetic regulation of the chromatin function in the nucleus raise an outstanding question about how timely and precise supply/consumption of these metabolites is achieved in the nucleus. We report here the identification of a nonclassical TCA cycle in the nucleus (nTCA cycle). We found that all the TCA cycle-associated enzymes including citrate synthase (CS), aconitase 2 (ACO2), isocitrate dehydrogenase 3 (IDH3), oxoglutarate dehydrogenase (OGDH), succinyl-CoA synthetase (SCS), fumarate hydratase (FH), and malate dehydrogenase 2 (MDH2), except for succinate dehydrogenase (SDH), a component of electron transport chain for generating ATP, exist in the nucleus. We showed that these nuclear enzymes catalyze an incomplete TCA cycle similar to that found in cyanobacteria. We propose that the nTCA cycle is implemented mainly to generate/consume metabolic intermediates, not for energy production. We demonstrated that the nTCA cycle is intrinsically linked to chromatin dynamics and transcription regulation. Together, our study uncovers the existence of a nonclassical TCA cycle in the nucleus that links the metabolic pathway to epigenetic regulation.

Staphylococcus aureus biofilm matrix under bone environment influence

2020 ◽  
Author(s):  
Fabien Lamret ◽  
Jennifer Varin-Simon ◽  
Sophie Gangloff ◽  
Fany Reffuveille
Keyword(s):  
Staphylococcus Aureus ◽  
Bacterial Adhesion ◽  
Biofilm Formation ◽  
Matrix Composition ◽  
Magnesium Concentration ◽  
Bone Microenvironment ◽  
Low Oxygen ◽  
The Matrix ◽  
Main Components ◽  
Biofilm Matrix

&lt;p&gt;Bone and joint infections linked to implanted materials are mostly due to Staphylococcus aureus. Deciphering the biofilm structure appears to be a promising strategy to develop antibiofilm molecules in order to curb infection occurrence and the bacterial recurrence. Indeed, the characterization of biofilm architecture and physiology could help to find new therapeutic targets through notable quantification of the matrix main components. Our hypothesis is that the very complex and interconnected bone microenvironment influences the bacterial adhesion and biofilm maturation and so its composition.&lt;/p&gt; &lt;p&gt;To identify the main factors influencing biofilm formation in the bone microenvironment, we determined biofilm biomass and the number of live adhered bacteria in a static model, completed with microscopy approaches to support our results. Different factors of bone microenvironment were tested: starvation, low oxygen rate, excess of magnesium, and presence of bone cell products. Our first results showed that MSSA or MRSA strains did not have the same behaviors under the tested conditions. However, for both types of strains, excess of magnesium combined to paucity of amino acids and oxygen increased the most the proportion of adhered Staphylococcus aureus (a 6 to 43 fold-increase, p = &lt; 0.01). But biofilm biomass quantification and bacterial adhesion results showed divergent profiles leading us to think that matrix could be involved in such contrasts. Scanning electron microscopy highlighted several structures of matrix produced by these bacteria: well-known slime aspect, but also fibrous appearance, and no matrix production was revealed under some conditions. Indeed, all strains produced few matrix when cultured with control medium and oxygenated condition. Only CIP 53.154 strain built a strong slime-like matrix in response to oxygen depletion. However, both MSSA CIP 53.154 and SH1000 strains developed fibrous structures under anaerobic conditions associated with amino acid starvation, high magnesium concentration with or without glucose. MRSA USA300 strain did not seem to produce a matrix under our conditions, which is supported by the literature. Further investigations of the biofilm matrix are needed to conclude on the matrix nature, which surrounds bacteria under our conditions.&lt;/p&gt; &lt;p&gt;The bone microenvironment is complex but our results show that the parameters that mimicked this specific environment influenced the bacterial adhesion and probably the biofilm matrix composition of several strains of Staphylococcus aureus. Further investigations will help to understand how the different factors influence biofilm formation through quantification of the matrix main components by fluorescence microscopy and enzyme digestion. Our final aim is to develop an in vitro model mimicking this specific microenvironment in order to screen different antimicrobial molecules, which could target the biofilm matrix.&lt;/p&gt;

scholarly journals Disruption of the TCA cycle reveals an ATF4-dependent integration of redox and amino acid metabolism

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Dylan Gerard Ryan ◽  
Ming Yang ◽  
Hiran A Prag ◽  
Giovanny Rodriguez Blanco ◽  
Efterpi Nikitopoulou ◽  
...  
Keyword(s):  
Amino Acid ◽  
Amino Acid Metabolism ◽  
Acid Metabolism ◽  
Metabolic Response ◽  
Tricarboxylic Acid Cycle ◽  
Fumarate Hydratase ◽  
Tca Cycle ◽  
Comparative Approach ◽  
Redox Biology ◽  
The Tca Cycle

The Tricarboxylic Acid Cycle (TCA) cycle is arguably the most critical metabolic cycle in physiology and exists as an essential interface coordinating cellular metabolism, bioenergetics, and redox homeostasis. Despite decades of research, a comprehensive investigation into the consequences of TCA cycle dysfunction remains elusive. Here, we targeted two TCA cycle enzymes, fumarate hydratase (FH) and succinate dehydrogenase (SDH), and combined metabolomics, transcriptomics, and proteomics analyses to fully appraise the consequences of TCA cycle inhibition (TCAi) in murine kidney epithelial cells. Our comparative approach shows that TCAi elicits a convergent rewiring of redox and amino acid metabolism dependent on the activation of ATF4 and the integrated stress response (ISR). Furthermore, we also uncover a divergent metabolic response, whereby acute FHi, but not SDHi, can maintain asparagine levels via reductive carboxylation and maintenance of cytosolic aspartate synthesis. Our work highlights an important interplay between the TCA cycle, redox biology and amino acid homeostasis.

Effect of thermal injury on the TCA cycle enzymes of Staphylococcus aureus MF 31 and Salmonella typhimurium 7136

1971 ◽  
Vol 17 (6) ◽  
pp. 759-765 ◽  
Author(s):  
Richard I. Tomlins ◽  
Merle D. Pierson ◽  
Z. John Ordal
Keyword(s):  
Lactate Dehydrogenase ◽  
Malate Dehydrogenase ◽  
Thermal Injury ◽  
Specific Activity ◽  
Fumarate Hydratase ◽  
Tca Cycle ◽  
Tca Cycle Enzymes ◽  
The Tca Cycle ◽  
Oxoglutarate Dehydrogenase ◽  
Metabolic Activities

The heating of S. aureus MF-31 and S. typhimurium 7136 at 52C and 48C respectively, produced a sublethal heat injury. When injured cells were placed in fresh growth medium they recovered. The recovery of S. aureus was not inhibited by chloramphenicol. The metabolic activities of tricarboxylic acid (TCA) cycle enzymes, as well as other selected enzymes in crude extracts of normal and heat-injured cells of both microorganisms were assayed. In extracts from S. typhimurium there was some loss of specific activity with fumarate hydratase, glutamate dehydrogenase, fructose diphosphate aldolase, lactate dehydrogenase, and the NAD(P) oxidases as a result of heating. In extracts from S. aureus oxoglutarate dehydrogenase, malate dehydrogenase and lactate dehydrogenase were severely inactivated after heating. Other enzymes in comparison were only moderately sensitive to heat. No significant increase in enzyme activity was observed in extracts from injured cells of either microorganism. Re-naturation of lactate dehydrogenase and malate dehydrogenase occurred during the recovery of S. aureus both in the presence and absence of chloramphenicol. No renaturation of oxoglutarate dehydrogenase was found under the same conditions.

scholarly journals RSM–GA Based Optimization of Bacterial PHA Production and In Silico Modulation of Citrate Synthase for Enhancing PHA Production

Biomolecules ◽  
2019 ◽  
Vol 9 (12) ◽  
pp. 872 ◽  
Author(s):  
Apoorva Rao ◽  
Shafiul Haque ◽  
Hesham A. El-Enshasy ◽  
Vineeta Singh ◽  
Bhartendu Nath Mishra
Keyword(s):  
Molecular Docking ◽  
Nitrogen Source ◽  
In Silico ◽  
Citrate Synthase ◽  
Tca Cycle ◽  
Management Approach ◽  
Carbon And Nitrogen ◽  
The Tca Cycle ◽  
Different Types ◽  
Pha Production

The inexhaustible nature and biodegradability of bioplastics like polyhydroxyalkanoates (PHAs) make them suitable assets to replace synthetic plastics. The eventual fate of these eco-friendly and non-toxic bioplastics relies upon the endeavors towards satisfying cost and, in addition, execution necessity. In this study, we utilized and statistically optimized different food (kitchen-/agro-) waste as a sole carbon/nitrogen source for the production of PHA at a reduced cost, indicating a proficient waste administration procedure. Seven different types of kitchen-/agro-waste were used as unique carbon source and four different types of nitrogen source were used to study their impact on PHA production by Bacillus subtilis MTCC 144. Among four different studied production media, mineral salt medium (MSM) (biomass: 37.7 g/L; cell dry weight: 1.8 g/L; and PHA: 1.54 g/L) was found most suitable for PHA production. Further, carbon and nitrogen components of MSM were optimized using one-factor-at-a-time experiments, and found that watermelon rind (PHA = 12.97 g/L) and pulse peel (PHA = 13.5 g/L) were the most suitable carbon and nitrogen sources, respectively, in terms of PHA (78.60%) recovery. The concentrations of these factors (sources) were statistically optimized using response surface methodology coupled with the genetic algorithm approach. Additionally, in order to enhance microbial PHA production, the interaction of citrate synthase, a key enzyme in the TCA cycle, with different known inhibitors was studied using in silico molecular docking approach. The inhibition of citrate synthase induces the blockage of the tricarboxylic cycle (TCA), thereby increasing the concentration of acetyl-CoA that helps in enhanced PHA production. Molecular docking of citrate synthase with different inhibitors of PubChem database revealed that hesperidin (PubChem compound CID ID 10621), generally present in citrus fruits, is the most efficient inhibitor of the TCA cycle with the binding score of –11.4 and warrants experimental validation. Overall, this study provides an efficient food waste management approach by reducing the production cost and enhancing the production of PHA, thereby lessening our reliance on petroleum-based plastics.

scholarly journals Disruption of the TCA cycle reveals an ATF4-dependent integration of redox and amino acid metabolism

2021 ◽  
Author(s):  
Dylan Gerard Ryan ◽  
Ming Yang ◽  
Hiran A Prag ◽  
Giovanny Rodriguez Blanco ◽  
Efterpi Nikitopoulou ◽  
...  
Keyword(s):  
Amino Acid ◽  
Amino Acid Metabolism ◽  
Acid Metabolism ◽  
Metabolic Response ◽  
Tricarboxylic Acid Cycle ◽  
Fumarate Hydratase ◽  
Tca Cycle ◽  
Comparative Approach ◽  
Redox Biology ◽  
The Tca Cycle

The Tricarboxylic Acid Cycle (TCA) cycle is arguably the most critical metabolic cycle in physiology and exists as an essential interface coordinating cellular metabolism, bioenergetics, and redox homeostasis. Despite decades of research, a comprehensive investigation into the consequences of TCA cycle dysfunction remains elusive. Here, we targeted two TCA cycle enzymes, fumarate hydratase (FH) and succinate dehydrogenase (SDH), and combined metabolomics, transcriptomics, and proteomics analyses to fully appraise the consequences of TCA cycle inhibition (TCAi) in kidney epithelial cells. Our comparative approach shows that TCAi elicits a convergent rewiring of redox and amino acid metabolism dependent on the activation of ATF4 and the integrated stress response (ISR). Furthermore, we also uncover a divergent metabolic response, whereby acute FHi, but not SDHi, can maintain asparagine levels via reductive carboxylation and maintenance of cytosolic aspartate synthesis. Our work highlights an important interplay between the TCA cycle, redox biology and amino acid homeostasis.

Decrypting the matrix: how interspecies interactions influence matrix in multispecies biofilm?

2020 ◽  
Author(s):  
Cristina Amador ◽  
Henriette L. Røder ◽  
Ute Kuhlicke ◽  
Thomas Neu ◽  
Mette Burmølle
Keyword(s):  
Single Species ◽  
Matrix Composition ◽  
Emergent Properties ◽  
Interspecies Interactions ◽  
Matrix Encoding ◽  
The Matrix ◽  
Static Conditions ◽  
Encoding Genes ◽  
Multispecies Biofilms ◽  
Biofilm Matrix

&lt;p&gt;The biofilm matrix contributes to the establishment of microbial cells on very diverse surfaces, stabilizing biofilms and providing cells with protection against multiple hostile conditions. Moreover, the biofilm matrix can also retain nutrients, enzymes or quorum sensing molecules, favoring the establishment of social interactions among biofilm cells. Functional bacterial amyloids are part of the biofilm structural components of various species, and they were previously proven to bind QS molecules and strengthen the matrix. Multiple studies have been conducted to characterize matrix determinants and their regulation in single species biofilms, while these remain scarcely understood in multispecies biofilms. We have previously isolated and characterized a soil-derived consortium composed of Xanthomonas retroflexus, Stenotrophomonas rhizophila, Microbacterium oxydans and Paenibacillus amylolyticus showing enhanced biofilm biomass and differential gene/protein expression specific of the four-species biofilm.&lt;/p&gt; &lt;p&gt;This study aimed at exploring the effect of interspecies interactions on biofilm matrix production in the four-species biofilm. We hypothesize that interspecies interactions may result in differential expression of matrix-encoding genes responsible for biofilm emergent properties.&lt;/p&gt; &lt;p&gt;We searched for matrix determinant homologues in X.retroflexus and combined different techniques for characterizing the matrix identity and expression in mono-, dual- and multispecies biofilms.&lt;/p&gt; &lt;p&gt;The fap amyloid operon, described in Pseudomonas as a biofilm-scaffold contributing element, was deleted in X. retroflexus, replaced in the four-species model and compared to the parental community for biofilm structure and adhesion capability. The fap mutant displayed poor substrate colonization in flow cells in both mono- and multispecies biofilms with relative filamentous structure compared to the parental strain/ consortium. However, adhesion did not significantly change under static conditions. To characterize matrix composition, we tested 78 different lectins in multispecies biofilms and identified five that bound to our samples. Interestingly, some matrix glycoconjugates were only produced in the consortium.&lt;/p&gt; &lt;p&gt;Our data suggest that loss of matrix components, such as the Fap amyloid, and the presence of other species, influences synergistic biofilm properties in the four-species consortium. Ongoing approaches involving localized expression of matrix-encoding genes and matrix proteomes will aid in identifying the mechanisms underlying emergent properties in the four-species biofilm.&lt;/p&gt; &lt;p&gt;&amp;#160;&lt;/p&gt;

scholarly journals An Electrostatic Net Model for the Role of Extracellular DNA in Biofilm Formation by Staphylococcus aureus

2015 ◽  
Vol 197 (24) ◽  
pp. 3779-3787 ◽  
Author(s):  
Vanina Dengler ◽  
Lucy Foulston ◽  
Alicia S. DeFrancesco ◽  
Richard Losick
Keyword(s):  
Staphylococcus Aureus ◽  
Biofilm Formation ◽  
Extracellular Dna ◽  
Matrix Proteins ◽  
Exogenous Dna ◽  
Content Type ◽  
Cytoplasmic Proteins ◽  
The Matrix ◽  
Biofilm Matrix

ABSTRACTStaphylococcus aureusis an important human pathogen that can form biofilms on various surfaces. These cell communities are protected from the environment by a self-produced extracellular matrix composed of proteins, DNA, and polysaccharide. The exact compositions and roles of the different components are not fully understood. In this study, we investigated the role of extracellular DNA (eDNA) and its interaction with the recently identified cytoplasmic proteins that have a moonlighting role in the biofilm matrix. These matrix proteins associate with the cell surface upon the drop in pH that naturally occurs during biofilm formation, and we found here that this association is independent of eDNA. Conversely, the association of eDNA with the matrix was dependent on matrix proteins. Both proteinase and DNase treatments severely reduced clumping of resuspended biofilms; highlighting the importance of both proteins and eDNA in connecting cells together. By adding an excess of exogenous DNA to DNase-treated biofilm, clumping was partially restored, confirming the crucial role of eDNA in the interconnection of cells. On the basis of our results, we propose that eDNA acts as an electrostatic net, interconnecting cells surrounded by positively charged matrix proteins at a low pH.IMPORTANCEExtracellular DNA (eDNA) is an important component of the biofilm matrix of diverse bacteria, but its role in biofilm formation is not well understood. Here we report that inStaphylococcus aureus, eDNA associates with cells in a manner that depends on matrix proteins and that eDNA is required to link cells together in the biofilm. These results confirm previous studies that showed that eDNA is an important component of theS. aureusbiofilm matrix and also suggest that eDNA acts as an electrostatic net that tethers cells together via the proteinaceous layer of the biofilm matrix.

scholarly journals Advantage of Upregulation of Succinate Dehydrogenase in Staphylococcus aureus Biofilms

2010 ◽  
Vol 192 (9) ◽  
pp. 2385-2394 ◽  
Author(s):  
Rosmarie Gaupp ◽  
Steffen Schlag ◽  
Manuel Liebeke ◽  
Michael Lalk ◽  
Friedrich Götz
Keyword(s):  
Staphylococcus Aureus ◽  
Acetic Acid ◽  
Succinate Dehydrogenase ◽  
Growth Medium ◽  
Tca Cycle ◽  
Defined Medium ◽  
Metabolome Analysis ◽  
Aerobic Conditions ◽  
Small Colony Variant ◽  
The Tca Cycle

ABSTRACT Previous studies have demonstrated that various tricarboxylic acid (TCA) cycle genes, particularly the succinate dehydrogenase genes (sdhCAB), are upregulated in Staphylococcus aureus biofilms. To better study the role of this enzyme complex, an sdhCAB deletion mutant (Δsdh) was constructed. Compared to the wild type (wt) the mutant was impaired in planktonic growth under aerobic conditions, excreted acetic acid could not be reused and accumulated continuously, succinate was excreted and found in the culture supernatant, and metabolome analysis with cells grown in chemically defined medium revealed reduced uptake/metabolism of some amino acids from the growth medium. Moreover, the mutant was able to counteract the steadily decreasing extracellular pH by increased urease activity. The addition of fumarate to the growth medium restored the wt phenotype. The mutant showed a small-colony variant (SCV)-like phenotype, a slight increase in resistance to various aminoglycoside antibiotics, and decreased pigmentation. The decreased growth under aerobic conditions is due to the interruption of the TCA cycle (indicated by the accumulation of succinate and acetic acid) with the consequence that many fewer reduction equivalents (NADH and FADH2) can fuel the respiratory chain. The results indicate that the TCA cycle is required for acetate and amino acid catabolism; its upregulation under biofilm conditions is advantageous under such nutrient- and oxygen-limited conditions.

scholarly journals Engineering central pathways for industrial-level (3R)-acetoin biosynthesis in Corynebacterium glutamicum

2020 ◽  
Author(s):  
Lingxue Lu ◽  
Yufeng Mao ◽  
Mengyun Kou ◽  
Zhenzhen Cui ◽  
Biao Jin ◽  
...  
Keyword(s):  
Corynebacterium Glutamicum ◽  
Citrate Synthase ◽  
Optical Purity ◽  
Value Added ◽  
Tca Cycle ◽  
Product Yield ◽  
The Tca Cycle ◽  
Acetoin Production ◽  
Industrial Level ◽  
Optically Pure

Abstract Background: Acetoin, especially the optically pure (3S)- or (3R)-enantiomer, is a high-value-added bio-based platform chemical and important potential pharmaceutical intermediate. Over the past decades, intense efforts have been devoted to the production of acetoin through green biotechniques. However, efficient and economical methods for the production of optically pure acetoin enantiomers are rarely reported. Previously, we systematically engineered the GRAS microorganism Corynebacterium glutamicum to efficiently produce (3R)-acetoin from glucose. Nevertheless, its yield and average productivity were still unsatisfactory for industrial bioprocesses.Results: In this study, cellular carbon fluxes in the acetoin producer CGR6 were further redirected toward acetoin synthesis using several metabolic engineering strategies, including blocking anaplerotic pathways, attenuating key genes of the TCA cycle and integrating additional copies of the alsSD operon into the genome. Among them, the combination of attenuation of citrate synthase and inactivation of phosphoenolpyruvate carboxylase showed a significant synergistic effect on acetoin production. Finally, the optimal engineered strain CGS11 produced a titer of 102.45 g/L acetoin with a yield of 0.419 g/g glucose at a rate of 1.86 g/L/h in a 5 L fermenter. The optical purity of the resulting (3R)-acetoin surpassed 95%.Conclusion: To the best of our knowledge, this is the highest titer of highly enantiomerically enriched (3R)-acetoin, together with a competitive product yield and productivity, achieved in a simple, green processes without expensive additives or substrates. This process therefore opens the possibility to achieve easy, efficient, economical and environmentally-friendly production of (3R)-acetoin via microbial fermentation in the near future.

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