Novel pathway for curcumin utilization found in diverse Gram-negative soil-dwelling bacteria with evidence of horizontal gene transfer

Background Bacteria are known to contain complex pathways to metabolize a plethora of recalcitrant compounds, especially in soil and gut microbiomes. Plant-derived polyphenols are often considered to be non-pharmaceutical antimicrobials that exist within both the soil and gut. Curcumin is the polyphenol active compound in turmeric root ( Curcuma longa ) and demonstrates anti-inflammatory, antioxidative, and anti-cancer properties. The NADPH-curcumin/dihydrocurcumin reductase gene ( curA ), yielding curcumin-reducing enzymatic activity, was previously discovered in the genomic DNA of Escherichia coli strains isolated from stool samples. We hypothesized that curA may also be present within soil-dwelling bacteria. Results In the current study, we isolated 15 Gram-negative soil-dwelling bacteria with the highly conserved curA gene, using growth selection strategies including Winogradsky columns and Rapid Flask Cultures containing turmeric powder. Using in silico syntropy analysis, we found that curA is one gene within a highly conserved synteny cluster of 13 genes ( ydcU , ydcV , patD ( ddpA ), yncL , ortT , ydcY , ydcZ , mnaT ( mddA ), curA , mcbR ( gntR ), yncD ( fecA ), yncE , and ansP ) encoding metabolic-related proteins including enzymes, transport systems, and genetic regulators. Reverse-transcriptase quantitative PCR (RT-qPCR) analysis showed curA and 12 metabolic genes within the synteny cluster were significantly upregulated during 48 hr-growth with 1% turmeric in E. coli str. K12 substr. DC10B (positive control strain) and soil-isolated Chryseobacterium sp . Notably, ATR-FTIR data supported preferential cell-associated accumulation/retention of curcuminoid-derived material consistent with uptake and metabolism. Metatranscriptomics analysis of soil-turmeric growth slurries revealed a metabolic framework in which curcumin-derived carbon is likely assimilated into central metabolism while nitrogen-containing intermediates are redirected towards amino acid biosynthesis. In addition, within the same soil-turmeric slurries, we observed potential horizontal gene transfer through the absolute quantification of putative type IV and type VI secretion system genes. Conclusions Collectively, our data suggests a novel metabolic pathway for curcumin utilization in Gram-negative bacteria that is a conserved mobile genetic element.