Simultaneous hydrolysis and xylose conversion of wheat bran to glucose by Flammulina filiformis and its application in acetoin production using Bacillus subtilis

Hexose and pentose constitute the primary components in biomass hydrolysates regardless of chemical/biological hydrolysis, which impacts fermentative efficiency by industrial strains partially due to the existence of pentose. This study demonstrated Flammulina filiformis effectively hydrolyzed wheat bran (WB) to produce reducing sugars predominantly composed of glucose with minimal xylose. Furthermore, carbon utilization assays and multi-omics confirmed F. filiformis ' unique capability to convert xylose into glucose via gluconeogenesis, indicating concurrent hydrolysis and xylose conversion during the WB degradation. Process optimization by F. filiformis achieved maximum total reducing sugar (TRS) of 13.99 g/L (47.50% glucose and 3.95% xylose), while 19.48 g/L TRS by chemical hydrolysis contained 69.12% xylose and only 14.32% glucose. Remarkably, F. filiformis hydrolysates contained only phenolic compounds as fermentation inhibitors with negligible furfural, formic acid, and acetic acid. The WB hydrolysate by F. filiformis exhibited superior performance of growth rate and sugar consumption as well as acetoin production by Bacillus subtilis BS4481 compared with glucose, xylose or the chemical WB hydrolysate. Ultimately, fed-batch experiment afforded a maximum acetoin concentration of 86.65 g/L with 0.59 g/g yield. These results showed F. filiformis as a promising biocatalyst could be used for lignocellulosic biomass pretreatment and high-quality hydrolysate production for industrial applications. • Efficient hydrolysis of wheat bran into reducing sugar by Flammulina filiformis with the yield of 23.34%. • Glucose could be achieved from xylose via gluconeogenesis during the wheat bran hydrolysis process by F. filiformis . • BWBH demonstrated a superior fermentative performance over glucose/xylose and CWBH. • Bacillus subtilis BS4481 using BWBH as carbon source achieves an acetoin titer of 86.65 g/L (yield 0.59 g/g).