Multi-omics analysis of a traditional fermented food reveals byproduct-associated fungal strains for waste-to-food upcycling

Fungal solid state fermentation (SSF) of byproducts has promise for increasing food sustainability and security, but fungal waste-to-food conversion remains poorly understood at the genetic and molecular level. Here we use multi-omics to characterize red oncom, an Indonesian fermented food produced from the globally abundant byproduct of soy milk production (okara). We find that oncom is dominated by the filamentous fungus Neurospora intermedia, which uses an arsenal of carbohydrate-active enzymes to degrade pectin and cellulose to support its growth during the fermentation process. Strains used for oncom belong to a genetically distinct subpopulation that is associated with plant-based byproducts of human activity. In addition to encoding expanded hydrolytic capacity and mutations in diverse genes, byproduct-associated strains have higher secreted cellulase activity. Finally, N. intermedia grows on diverse industrially relevant byproducts and does not encode for any known mycotoxins, suggesting a promising growth and safety profile for potential applications beyond the context in which N. intermedia is traditionally used. Taken together, these results shed light on human domestication of microbes for fermented foods, enhance our molecular understanding of fungal waste-to-food conversion, and establish N. intermedia as a promising organism for byproduct upcycling in SSF and beyond