Fungal Interactions Strengthen the Diversity-Functioning Relationship of Solid-State Fermentation Systems

Abstract

Traditional fermentation processes are driven by complex fungal microbiomes. However, the exact means by which fungal diversity affects fermentation remains unclear. In this study, we systematically investigated the diversity of a fungal community and its functions during the multibatch <i>Baijiu</i> fermentation process. Metabolomics analysis showed that the metabolic profiles of the <i>Baijiu</i> were enhanced with an increase in the fermentation time, as determined from the characteristic volatile flavors. High-throughput sequencing technology revealed that the major fungal species involved in sauce-flavor <i>Baijiu</i> fermentation are <i>Pichia</i> sp. (41.75%, average relative abundance), <i>Saccharomyces</i> sp. (13.07%), thermophilic species (9.16%), <i>Monascus</i> sp. (6.80%), Aspergillus sp. (4.69%), <i>Schizosaccharomyces</i> sp. (3.76%), <i>Thermomyces</i> sp. (3.74%), and Zygosaccharomyces sp. (1.41%). In addition, the fungal diversity increased as the number of fermentation batches increased. Moreover, the increased fungal diversity contributed to the modularity of the fungal communities, wherein <i>Pichia</i> sp., <i>Torulaspora</i> sp., and <i>Saccharomyces</i> sp. maintained the stability of the fungal community. In addition, metatranscriptomics sequencing technologies were used to reconstruct the key metabolic pathways during fermentation, and it was found that the increased microbial diversity significantly promoted glucose-mediated carbon metabolism. Finally, functional gene analysis showed that functional microorganisms, such as Zygosaccharomyces and <i>Pichia</i>, can enhance fermentation as a result of the high expression of pyruvate decarboxylase and propanol-preferring alcohol dehydrogenase during the metabolism of pyruvate. These results indicate that fungal biodiversity can be exploited to enhance fermentation-based processes via network interactions and metabolism during multiple-batch fermentation. <b>IMPORTANCE</b> Biodiversity and network interactions act simultaneously on the microbial community structure in the <i>Baijiu</i> fermentation process, thereby rendering the microbiome dynamics challenging to manage and predict. Understanding the complex fermentation community and its relationship to community functions is therefore important in the context of developing improved fermentation biotechnology systems. Our work demonstrates that multiple-batch fermentation steps increase microbial diversity and promote community stability. Crucially, the enhanced modularity in the microbial network increases the metabolism of flavor compounds and ethanol. This study highlights the power of biodiversity and network interactions in regulating the function of the microbiome in food fermentation ecosystems.