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

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 Baijiu ferme...

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Autores principales: Zhang, Hongxia, Tan, Yuwei, Wei, Junlin, Du, Hai, Xu, Yan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9426468/
https://www.ncbi.nlm.nih.gov/pubmed/35862822
http://dx.doi.org/10.1128/msystems.00401-22
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author Zhang, Hongxia
Tan, Yuwei
Wei, Junlin
Du, Hai
Xu, Yan
author_facet Zhang, Hongxia
Tan, Yuwei
Wei, Junlin
Du, Hai
Xu, Yan
author_sort Zhang, Hongxia
collection PubMed
description 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 Baijiu fermentation process. Metabolomics analysis showed that the metabolic profiles of the Baijiu 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 Baijiu fermentation are Pichia sp. (41.75%, average relative abundance), Saccharomyces sp. (13.07%), thermophilic species (9.16%), Monascus sp. (6.80%), Aspergillus sp. (4.69%), Schizosaccharomyces sp. (3.76%), Thermomyces 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 Pichia sp., Torulaspora sp., and Saccharomyces 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 Pichia, 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. IMPORTANCE Biodiversity and network interactions act simultaneously on the microbial community structure in the Baijiu 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.
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spelling pubmed-94264682022-08-31 Fungal Interactions Strengthen the Diversity-Functioning Relationship of Solid-State Fermentation Systems Zhang, Hongxia Tan, Yuwei Wei, Junlin Du, Hai Xu, Yan mSystems Research Article 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 Baijiu fermentation process. Metabolomics analysis showed that the metabolic profiles of the Baijiu 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 Baijiu fermentation are Pichia sp. (41.75%, average relative abundance), Saccharomyces sp. (13.07%), thermophilic species (9.16%), Monascus sp. (6.80%), Aspergillus sp. (4.69%), Schizosaccharomyces sp. (3.76%), Thermomyces 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 Pichia sp., Torulaspora sp., and Saccharomyces 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 Pichia, 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. IMPORTANCE Biodiversity and network interactions act simultaneously on the microbial community structure in the Baijiu 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. American Society for Microbiology 2022-07-05 /pmc/articles/PMC9426468/ /pubmed/35862822 http://dx.doi.org/10.1128/msystems.00401-22 Text en Copyright © 2022 Zhang et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Zhang, Hongxia
Tan, Yuwei
Wei, Junlin
Du, Hai
Xu, Yan
Fungal Interactions Strengthen the Diversity-Functioning Relationship of Solid-State Fermentation Systems
title Fungal Interactions Strengthen the Diversity-Functioning Relationship of Solid-State Fermentation Systems
title_full Fungal Interactions Strengthen the Diversity-Functioning Relationship of Solid-State Fermentation Systems
title_fullStr Fungal Interactions Strengthen the Diversity-Functioning Relationship of Solid-State Fermentation Systems
title_full_unstemmed Fungal Interactions Strengthen the Diversity-Functioning Relationship of Solid-State Fermentation Systems
title_short Fungal Interactions Strengthen the Diversity-Functioning Relationship of Solid-State Fermentation Systems
title_sort fungal interactions strengthen the diversity-functioning relationship of solid-state fermentation systems
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9426468/
https://www.ncbi.nlm.nih.gov/pubmed/35862822
http://dx.doi.org/10.1128/msystems.00401-22
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