Volatile Organic Compound-Mediated Antifungal Activity of <i>Pichia</i> spp. and Its Effect on the Metabolic Profiles of Fermentation Communities

Abstract

Volatile organic compounds (VOCs) are chemicals responsible for antagonistic activity between microorganisms. The impact of VOCs on microbial community succession of fermentation is not well understood. In this study, <i>Pichia</i> spp. were evaluated for VOC production as a part of antifungal activity during baijiu fermentation. The results showed that the abundance of <i>Pichia</i> in the defect group (agglomerated fermented grains) was lower than that in control group, and a negative interaction between <i>Pichia</i> and <i>Monascus</i> was determined (<i>P < </i>0.05). In addition, the disruption of fungi was significantly related to the differences of metabolic profiles in fermented grains. To determine production of VOCs from <i>Pichia</i> and its effect on <i>Monascus purpureus</i>, a double-dish system was assessed, and the incidence of <i>M. purpureus</i> reduction was 39.22% after 7 days. As to antifungal volatile compounds, 2-phenylethanol was identified to have an antifungal effect on <i>M. purpureus</i> through contact and noncontact. To further confirm the antifungal activity of 2-phenylethanol, scanning electron microscopy showed that 2-phenylethanol widely and significantly inhibited conidium germination and mycelial growth of filamentous fungi. Metatranscriptomic analysis revealed that the Ehrlich pathway is the metabolic path of 2-phenylethanol in <i>Pichia</i> and identified potential antifungal mechanisms, including protein synthesis and DNA damage. This study demonstrated the role of volatile compound-mediated microbial interaction in microbiome assembly and discovered a plausible scenario in which <i>Pichia</i> antagonized fungal blooms. The results may improve the niche establishment and growth of the functional yeast that enhances the flavor of baijiu.<b>IMPORTANCE</b> Fermentation of food occurs within communities of interacting species. The importance of microbial interactions in shaping microbial structure and metabolic performance to optimize the traditional fermentation process has long been emphasized, but the interaction mechanisms remain unclear. This study applied metabolome analysis and amplicon sequencing along with metatranscriptomic analysis to examine the volatile organic compound-mediated antifungal activity of <i>Pichia</i> and its effect on the metabolism of ethanol during baijiu fermentation, potentially enhancing the establishment of the fermentation niche and improving ethanol metabolism.