Integrated untargeted metabolomics and transcriptomics revealed the high-efficiency synthesis of theabrownins by Pantoea camelliae Z09 in liquid-state fermentation

Theabrownins (TBs) are complex macromolecular polymers with notable health benefits and considerable market potential, making their efficient and large-scale production essential. Our preliminary screening identified Pantoea camelliae Z09 liquid-state fermentation as an effective strategy for TBs synthesis. In this study, high-efficiency TBs synthesis was investigated by integrating untargeted metabolomics and transcriptomics. Within 48 h, the tea infusion color changed from bright light orange to oily brown-black, corresponding to TBs accumulation. At 48 h, the TBs concentration reached 12.57 mg/mL, representing a relatively high level. Structural analysis at 24, 36, and 48 h showed that TBs mainly consist of phenols, proteins, sugars, and lipids, with hydroxyl, carboxyl, and amino groups as the dominant functional groups. During fermentation, the pH of the tea infusion increased overall, consistent with the changes observed in the TBs solution. Quantitative profiling identified 322 key compounds and 145 differential genes involved in TBs synthesis, including phenylpropanoids, polyketides, and genes encoding hydrolases, transferases, and oxidoreductases. Seven catechins (C, EC, GC, EGC, ECG, GCG, and EGCG) were confirmed as major contributors to TBs formation, while the addition of quercetin and glucose, gallic acid, hesperidin, and apigenin further enhanced TBs production. This study provides theoretical guidance for efficient large-scale TBs production and establishes a paradigm for elucidating microbe-driven macromolecular synthesis. • P. camelliae Z09 was the functional microorganism to synthesize TBs efficiently. • Efficient TBs synthesis of 12.57 mg/mL within 48 h. • 145 genes, including oxidoreductase genes, positively correlated with TBs synthesis. • 322 compounds negatively correlated with TBs synthesis, with 7 catechins as key components. • A mixture of catechins, quercetin, and glucose enhanced TBs synthesis ( p <0.05).