Synergistic effect in core microbiota associated with sulfur metabolism in spontaneous Chinese liquor fermentation

Abstract

Microbial sulfur metabolism plays crucial roles in various food and alcoholic beverage fermentations. 3-(Methylthio)-1-propanol and dimethyl disulfide are important sulfur compounds in fermented foods and alcoholic beverages. Here, we studied the dynamics of these two compounds during spontaneous Chinese liquor fermentation. The two compounds reached the maximum concentration at day 10 and the maximum production rate at day 3. Metatranscriptomic analysis at days 3 and 10 revealed a total of 354 metabolically active microorganisms. Saccharomyces and Lactobacillus were identified as core microbiota critical for sulfur compound production based on both the transcript abundances of the principal genes and the distribution frequencies of 31 enzymes involved in sulfur metabolism. Saccharomyces transcribed genes encoding 23 enzymes related to the generation of 3-(methylthio)- 1-propanol and dimethyl disulfide, and Lactobacillus was active in the methyl cycle, which recycles methionine, the precursor of the two sulfur compounds. Furthermore, the sulfur metabolism-related characteristics of two representative species were studied in coculture during a simulated fermentation. Saccharomyces cerevisiae JZ109 produced 158.4 μg/liter 3-(methylthio)-1-propanol and 58.5 μg/liter dimethyl disulfide in monoculture, whereas Lactobacillus buchneri JZ-JN-2017 could not produce these two compounds in monoculture. Their coculture significantly enhanced the generation of 3-(methylthio)-1-propanol (350.0 μg/liter) and dimethyl disulfide (123.8 μg/liter). In addition, coculture significantly enhanced the gene transcriptions (fold change, 1.5 to 55.0) that convert methionine to these two compounds in S. cerevisiae and in the methyl cycle of L. buchneri. This study reveals a novel synergistic effect between members of the core microbiota in the production of sulfur compounds via methionine recycling in spontaneous Chinese liquor fermentation.