Deciphering Succession and Assembly Patterns of Microbial Communities in a Two-Stage Solid-State Fermentation System

Abstract

ABSTRACT Although the importance of microbiota in the natural environment and in industrial production has been widely recognized, little is known about the formation and succession patterns of the microbial community, particularly secondary succession after disturbance. Here, we choose the Xiaoqu liquor brewing process as an experimental model in which sorghum grains were first aerobically saccharified and then anaerobically fermented after being stirred and acidified to explore multistage community succession patterns. We analyzed microbial composition, physicochemical factors, and metabolites of brewing grains inoculated with two different starters, pure starter and traditional starter, respectively. Two groups showed similar succession patterns where the saccharification microbiota was mainly derived from starters, while environmental microorganisms, mainly Lactobacillaceae and Saccharomyces, dominated the fermentation microbiota regardless of the original saccharification community composition. Species replacement shaped the bacterial community, while species replacement and loss both contributed to fungal community succession in both groups. Grain acidification and hypoxia led to the succession of bacterial and fungal communities during fermentation, respectively. Despite inoculation with starters containing different microorganisms, similar microbial communities during the fermentation stage of the two groups exhibited similar metabolite composition. However, higher abundance of Rhizopus in the saccharification of the pure starter group led to more alcohols, while higher abundance of Monascus and Saccharomycopsis in the traditional starter group promoted acid and ester metabolism. These results revealed the microbial succession patterns of two-stage liquor brewing and its influence on flavor metabolism, which could be used to regulate the microbial community in food fermentation to further promote the modernization of the fermented food industry. IMPORTANCE Revealing formation and assembly mechanisms of microbiota can help us to understand and further regulate its roles in the ecosystems. The Xiaoqu liquor brewing system is a tractable microbial ecosystem with low complexity. This two-stage microbial ecosystem can be used as an experimental model to analyze the multistage temporal succession pattern of microbial communities. Our results demonstrated the dynamic composition and succession pattern of a microbial community in the two-stage liquor brewing system. The results also revealed the microbial origins determining community composition, the ecological processes dominating microbial community succession patterns, the determinants affecting microbial community successions, and the effect of microbial community changes on metabolite synthesis. Overall, our study not only provides an insight into multistage succession patterns of microbial communities in liquor brewing systems but also provides reference for optimizing the quality of fermented products, which will be helpful to understand the succession patterns of microbial communities in other natural ecosystems.

Keywords

• Xiaoqu liquor
• community succession
• turnover
• nestedness
• community assembly