Pediococcus spp. - mediated competition interaction within Daqu microbiota determines the temperature formation and metabolic profiles
Fermented microbiota is critical to the formation of microenvironment and metabolic profiles in spontaneous fermentation. Microorganisms generate a diverse array of metabolites concurrent with the release of heat energy. In the case of Daqu fermentation, the peak temperature exceeded 60°C, forming a...
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description | Fermented microbiota is critical to the formation of microenvironment and metabolic profiles in spontaneous fermentation. Microorganisms generate a diverse array of metabolites concurrent with the release of heat energy. In the case of Daqu fermentation, the peak temperature exceeded 60°C, forming a typical high-temperature fermentation system known as high-temperature Daqu. However, microorganisms that cause the quality variation in Daqu and how they affect the functional microbiota and microenvironment in the fermentation process are not yet clear. This study adopted high-throughput sequencing and monitored the dynamic fluctuations of metabolites and environmental factors to identify the pivotal microorganism responsible for the alterations in interaction patterns of functional keystone taxa and quality decline in the fermentation system of different operational areas during the
fermentation process that had been mainly attributed to operational taxonomic unit (OTU)_22 (
). Additionally, we used isothermal microcalorimetry, plate inhibition experiments, and
simulation fermentation experiments to explore the impact of
spp. on heat generation, microorganisms, and metabolite profiles. Results showed the heat peak generated by
spp. was significantly lower than that of
spp., filamentous fungi, and yeast. In addition, the preferential growth of
strain AA3 would obviously affect other strains to colonize through competition, and its metabolites made a significant impact on filamentous fungi. The addition of
strain AA3 in simulated fermentation would cause the loss of pyrazines and acids in metabolites. These evidences showed that the overgrowth of
spp. greatly influenced the formation of high temperatures and compounds in solid-state fermentation systems. Our work illustrated the vital impact of interaction variability mediated by
spp. for microbial assembly and metabolites, as well as in forming temperature. These results emphasized the functional role of Daqu microbiota in metabolites and heat production and the importance of cooperation in improving the fermentation quality.IMPORTANCEThe stable and high-quality saccharifying and fermenting starter in traditional solid-state fermentation was the prerequisite for liquor brewing. An imbalance of microbial homeostasis in fermentation can adversely impact production quality. Identification of such critical microorganisms and verifying their associations with other fermentation parameters pose a challenge in a tra |
doi_str_mv | 10.1128/aem.01790-23 |
format | Article |
fullrecord | <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_11022566</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>3054207313</sourcerecordid><originalsourceid>FETCH-LOGICAL-a404t-df3e97ebc1550984e36f0a98feb8a30e11c254ae94a18359d30db45c1faf603e3</originalsourceid><addsrcrecordid>eNp1kU1v1DAQhi0EokvhxhlZ4gISWcZ2nI1PCJVPqRIc4GxNnAnrKolT2wHxB_jduLulfEicPLKfecfvvIw9FLAVQrbPkaYtiJ2BSqpbbCPAtJVWqrnNNgDGVFLWcMLupXQBADU07V12oloNjZZiw358pN4HF5xbE0_LsuUVn8oVZuq5C9NC2WcfZu7nTBHdof7m897P_BVernzyLobOh4y8p4JMfqbE8554ptIdMa-R-BDihIdenPsyIGMXRu_4EsPgR0r32Z0Bx0QPrs9T9vnN609n76rzD2_fn708r7CGOlf9oMjsqHNC6-KzJtUMgKYdqGtRAQnhpK6RTI2iVdr0Cvqu1k4MODSgSJ2yF0fdZe2KTUdzjjjaJfoJ43cb0Nu_X2a_t1_CVysESKmbpig8uVaI4XKllO3kk6NxxJnCmqw0O7kDaYQp6ON_0Iuwxrn4swp0LWGnhCrUsyNV9phSpOHmNwLsVcK2JGwPCVt5hT894pgm-VvwP-yjP93eCP-KX_0EIFSyRg</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>3054207313</pqid></control><display><type>article</type><title>Pediococcus spp. - mediated competition interaction within Daqu microbiota determines the temperature formation and metabolic profiles</title><source>American Society for Microbiology</source><source>PubMed Central</source><source>Alma/SFX Local Collection</source><creator>Wu, Shenglu ; Lu, Jun ; Li, Changwen ; Du, Hai ; Xu, Yan</creator><contributor>Ercolini, Danilo</contributor><creatorcontrib>Wu, Shenglu ; Lu, Jun ; Li, Changwen ; Du, Hai ; Xu, Yan ; Ercolini, Danilo</creatorcontrib><description>Fermented microbiota is critical to the formation of microenvironment and metabolic profiles in spontaneous fermentation. Microorganisms generate a diverse array of metabolites concurrent with the release of heat energy. In the case of Daqu fermentation, the peak temperature exceeded 60°C, forming a typical high-temperature fermentation system known as high-temperature Daqu. However, microorganisms that cause the quality variation in Daqu and how they affect the functional microbiota and microenvironment in the fermentation process are not yet clear. This study adopted high-throughput sequencing and monitored the dynamic fluctuations of metabolites and environmental factors to identify the pivotal microorganism responsible for the alterations in interaction patterns of functional keystone taxa and quality decline in the fermentation system of different operational areas during the
fermentation process that had been mainly attributed to operational taxonomic unit (OTU)_22 (
). Additionally, we used isothermal microcalorimetry, plate inhibition experiments, and
simulation fermentation experiments to explore the impact of
spp. on heat generation, microorganisms, and metabolite profiles. Results showed the heat peak generated by
spp. was significantly lower than that of
spp., filamentous fungi, and yeast. In addition, the preferential growth of
strain AA3 would obviously affect other strains to colonize through competition, and its metabolites made a significant impact on filamentous fungi. The addition of
strain AA3 in simulated fermentation would cause the loss of pyrazines and acids in metabolites. These evidences showed that the overgrowth of
spp. greatly influenced the formation of high temperatures and compounds in solid-state fermentation systems. Our work illustrated the vital impact of interaction variability mediated by
spp. for microbial assembly and metabolites, as well as in forming temperature. These results emphasized the functional role of Daqu microbiota in metabolites and heat production and the importance of cooperation in improving the fermentation quality.IMPORTANCEThe stable and high-quality saccharifying and fermenting starter in traditional solid-state fermentation was the prerequisite for liquor brewing. An imbalance of microbial homeostasis in fermentation can adversely impact production quality. Identification of such critical microorganisms and verifying their associations with other fermentation parameters pose a challenge in a traditional fermentation environment. To enhance the quality of spontaneous fermented products, strategies such as bioaugmentation or the control of harmful microorganisms would be employed. This work started with the differences in high-temperature Daqu metabolites to explore a series of functional microorganisms that could potentially contribute to product disparities, and found that the differences in interactions facilitated directly or indirectly by
spp. seriously affected the development of microbial communities and metabolites, as well as the formation of the microenvironment. This study not only identified functional microbiota in Daqu that affected fermentation quality, but also demonstrated how microorganisms interact to affect the fermentation system, which would provide guidance for microbial supervision in the actual production process. Besides, the application of isothermal microcalorimetry in this study was helpful for us to understand the heat production capacity of microorganisms and their adaptability to the environment. This study presented a commendable framework for improving and controlling the quality of traditional fermentation and inspired further investigations in similar systems.</description><identifier>ISSN: 0099-2240</identifier><identifier>ISSN: 1098-5336</identifier><identifier>EISSN: 1098-5336</identifier><identifier>DOI: 10.1128/aem.01790-23</identifier><identifier>PMID: 38506521</identifier><language>eng</language><publisher>United States: American Society for Microbiology</publisher><subject>Bacteria ; Environmental factors ; Fermentation ; Food Microbiology ; Fungi ; Heat ; Heat generation ; High temperature ; Metabolism ; Metabolites ; Microbiota ; Microenvironments ; Microorganisms ; Next-generation sequencing ; Pediococcus ; Solid state fermentation ; Temperature ; Yeasts</subject><ispartof>Applied and environmental microbiology, 2024-04, Vol.90 (4), p.e0179023</ispartof><rights>Copyright © 2024 American Society for Microbiology.</rights><rights>Copyright American Society for Microbiology Apr 2024</rights><rights>Copyright © 2024 American Society for Microbiology. 2024 American Society for Microbiology.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-a404t-df3e97ebc1550984e36f0a98feb8a30e11c254ae94a18359d30db45c1faf603e3</cites><orcidid>0000-0003-1268-932X ; 0000-0002-7380-6473 ; 0000-0002-7919-4762</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://journals.asm.org/doi/pdf/10.1128/aem.01790-23$$EPDF$$P50$$Gasm2$$H</linktopdf><linktohtml>$$Uhttps://journals.asm.org/doi/full/10.1128/aem.01790-23$$EHTML$$P50$$Gasm2$$H</linktohtml><link.rule.ids>230,314,723,776,780,881,3175,27901,27902,52726,52727,52728,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38506521$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Ercolini, Danilo</contributor><creatorcontrib>Wu, Shenglu</creatorcontrib><creatorcontrib>Lu, Jun</creatorcontrib><creatorcontrib>Li, Changwen</creatorcontrib><creatorcontrib>Du, Hai</creatorcontrib><creatorcontrib>Xu, Yan</creatorcontrib><title>Pediococcus spp. - mediated competition interaction within Daqu microbiota determines the temperature formation and metabolic profiles</title><title>Applied and environmental microbiology</title><addtitle>Appl Environ Microbiol</addtitle><addtitle>Appl Environ Microbiol</addtitle><description>Fermented microbiota is critical to the formation of microenvironment and metabolic profiles in spontaneous fermentation. Microorganisms generate a diverse array of metabolites concurrent with the release of heat energy. In the case of Daqu fermentation, the peak temperature exceeded 60°C, forming a typical high-temperature fermentation system known as high-temperature Daqu. However, microorganisms that cause the quality variation in Daqu and how they affect the functional microbiota and microenvironment in the fermentation process are not yet clear. This study adopted high-throughput sequencing and monitored the dynamic fluctuations of metabolites and environmental factors to identify the pivotal microorganism responsible for the alterations in interaction patterns of functional keystone taxa and quality decline in the fermentation system of different operational areas during the
fermentation process that had been mainly attributed to operational taxonomic unit (OTU)_22 (
). Additionally, we used isothermal microcalorimetry, plate inhibition experiments, and
simulation fermentation experiments to explore the impact of
spp. on heat generation, microorganisms, and metabolite profiles. Results showed the heat peak generated by
spp. was significantly lower than that of
spp., filamentous fungi, and yeast. In addition, the preferential growth of
strain AA3 would obviously affect other strains to colonize through competition, and its metabolites made a significant impact on filamentous fungi. The addition of
strain AA3 in simulated fermentation would cause the loss of pyrazines and acids in metabolites. These evidences showed that the overgrowth of
spp. greatly influenced the formation of high temperatures and compounds in solid-state fermentation systems. Our work illustrated the vital impact of interaction variability mediated by
spp. for microbial assembly and metabolites, as well as in forming temperature. These results emphasized the functional role of Daqu microbiota in metabolites and heat production and the importance of cooperation in improving the fermentation quality.IMPORTANCEThe stable and high-quality saccharifying and fermenting starter in traditional solid-state fermentation was the prerequisite for liquor brewing. An imbalance of microbial homeostasis in fermentation can adversely impact production quality. Identification of such critical microorganisms and verifying their associations with other fermentation parameters pose a challenge in a traditional fermentation environment. To enhance the quality of spontaneous fermented products, strategies such as bioaugmentation or the control of harmful microorganisms would be employed. This work started with the differences in high-temperature Daqu metabolites to explore a series of functional microorganisms that could potentially contribute to product disparities, and found that the differences in interactions facilitated directly or indirectly by
spp. seriously affected the development of microbial communities and metabolites, as well as the formation of the microenvironment. This study not only identified functional microbiota in Daqu that affected fermentation quality, but also demonstrated how microorganisms interact to affect the fermentation system, which would provide guidance for microbial supervision in the actual production process. Besides, the application of isothermal microcalorimetry in this study was helpful for us to understand the heat production capacity of microorganisms and their adaptability to the environment. This study presented a commendable framework for improving and controlling the quality of traditional fermentation and inspired further investigations in similar systems.</description><subject>Bacteria</subject><subject>Environmental factors</subject><subject>Fermentation</subject><subject>Food Microbiology</subject><subject>Fungi</subject><subject>Heat</subject><subject>Heat generation</subject><subject>High temperature</subject><subject>Metabolism</subject><subject>Metabolites</subject><subject>Microbiota</subject><subject>Microenvironments</subject><subject>Microorganisms</subject><subject>Next-generation sequencing</subject><subject>Pediococcus</subject><subject>Solid state fermentation</subject><subject>Temperature</subject><subject>Yeasts</subject><issn>0099-2240</issn><issn>1098-5336</issn><issn>1098-5336</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><recordid>eNp1kU1v1DAQhi0EokvhxhlZ4gISWcZ2nI1PCJVPqRIc4GxNnAnrKolT2wHxB_jduLulfEicPLKfecfvvIw9FLAVQrbPkaYtiJ2BSqpbbCPAtJVWqrnNNgDGVFLWcMLupXQBADU07V12oloNjZZiw358pN4HF5xbE0_LsuUVn8oVZuq5C9NC2WcfZu7nTBHdof7m897P_BVernzyLobOh4y8p4JMfqbE8554ptIdMa-R-BDihIdenPsyIGMXRu_4EsPgR0r32Z0Bx0QPrs9T9vnN609n76rzD2_fn708r7CGOlf9oMjsqHNC6-KzJtUMgKYdqGtRAQnhpK6RTI2iVdr0Cvqu1k4MODSgSJ2yF0fdZe2KTUdzjjjaJfoJ43cb0Nu_X2a_t1_CVysESKmbpig8uVaI4XKllO3kk6NxxJnCmqw0O7kDaYQp6ON_0Iuwxrn4swp0LWGnhCrUsyNV9phSpOHmNwLsVcK2JGwPCVt5hT894pgm-VvwP-yjP93eCP-KX_0EIFSyRg</recordid><startdate>20240417</startdate><enddate>20240417</enddate><creator>Wu, Shenglu</creator><creator>Lu, Jun</creator><creator>Li, Changwen</creator><creator>Du, Hai</creator><creator>Xu, Yan</creator><general>American Society for Microbiology</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QL</scope><scope>7QO</scope><scope>7SN</scope><scope>7SS</scope><scope>7ST</scope><scope>7T7</scope><scope>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>SOI</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-1268-932X</orcidid><orcidid>https://orcid.org/0000-0002-7380-6473</orcidid><orcidid>https://orcid.org/0000-0002-7919-4762</orcidid></search><sort><creationdate>20240417</creationdate><title>Pediococcus spp. - mediated competition interaction within Daqu microbiota determines the temperature formation and metabolic profiles</title><author>Wu, Shenglu ; Lu, Jun ; Li, Changwen ; Du, Hai ; Xu, Yan</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-a404t-df3e97ebc1550984e36f0a98feb8a30e11c254ae94a18359d30db45c1faf603e3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Bacteria</topic><topic>Environmental factors</topic><topic>Fermentation</topic><topic>Food Microbiology</topic><topic>Fungi</topic><topic>Heat</topic><topic>Heat generation</topic><topic>High temperature</topic><topic>Metabolism</topic><topic>Metabolites</topic><topic>Microbiota</topic><topic>Microenvironments</topic><topic>Microorganisms</topic><topic>Next-generation sequencing</topic><topic>Pediococcus</topic><topic>Solid state fermentation</topic><topic>Temperature</topic><topic>Yeasts</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wu, Shenglu</creatorcontrib><creatorcontrib>Lu, Jun</creatorcontrib><creatorcontrib>Li, Changwen</creatorcontrib><creatorcontrib>Du, Hai</creatorcontrib><creatorcontrib>Xu, Yan</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Environment Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>Environment Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Applied and environmental microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wu, Shenglu</au><au>Lu, Jun</au><au>Li, Changwen</au><au>Du, Hai</au><au>Xu, Yan</au><au>Ercolini, Danilo</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Pediococcus spp. - mediated competition interaction within Daqu microbiota determines the temperature formation and metabolic profiles</atitle><jtitle>Applied and environmental microbiology</jtitle><stitle>Appl Environ Microbiol</stitle><addtitle>Appl Environ Microbiol</addtitle><date>2024-04-17</date><risdate>2024</risdate><volume>90</volume><issue>4</issue><spage>e0179023</spage><pages>e0179023-</pages><issn>0099-2240</issn><issn>1098-5336</issn><eissn>1098-5336</eissn><abstract>Fermented microbiota is critical to the formation of microenvironment and metabolic profiles in spontaneous fermentation. Microorganisms generate a diverse array of metabolites concurrent with the release of heat energy. In the case of Daqu fermentation, the peak temperature exceeded 60°C, forming a typical high-temperature fermentation system known as high-temperature Daqu. However, microorganisms that cause the quality variation in Daqu and how they affect the functional microbiota and microenvironment in the fermentation process are not yet clear. This study adopted high-throughput sequencing and monitored the dynamic fluctuations of metabolites and environmental factors to identify the pivotal microorganism responsible for the alterations in interaction patterns of functional keystone taxa and quality decline in the fermentation system of different operational areas during the
fermentation process that had been mainly attributed to operational taxonomic unit (OTU)_22 (
). Additionally, we used isothermal microcalorimetry, plate inhibition experiments, and
simulation fermentation experiments to explore the impact of
spp. on heat generation, microorganisms, and metabolite profiles. Results showed the heat peak generated by
spp. was significantly lower than that of
spp., filamentous fungi, and yeast. In addition, the preferential growth of
strain AA3 would obviously affect other strains to colonize through competition, and its metabolites made a significant impact on filamentous fungi. The addition of
strain AA3 in simulated fermentation would cause the loss of pyrazines and acids in metabolites. These evidences showed that the overgrowth of
spp. greatly influenced the formation of high temperatures and compounds in solid-state fermentation systems. Our work illustrated the vital impact of interaction variability mediated by
spp. for microbial assembly and metabolites, as well as in forming temperature. These results emphasized the functional role of Daqu microbiota in metabolites and heat production and the importance of cooperation in improving the fermentation quality.IMPORTANCEThe stable and high-quality saccharifying and fermenting starter in traditional solid-state fermentation was the prerequisite for liquor brewing. An imbalance of microbial homeostasis in fermentation can adversely impact production quality. Identification of such critical microorganisms and verifying their associations with other fermentation parameters pose a challenge in a traditional fermentation environment. To enhance the quality of spontaneous fermented products, strategies such as bioaugmentation or the control of harmful microorganisms would be employed. This work started with the differences in high-temperature Daqu metabolites to explore a series of functional microorganisms that could potentially contribute to product disparities, and found that the differences in interactions facilitated directly or indirectly by
spp. seriously affected the development of microbial communities and metabolites, as well as the formation of the microenvironment. This study not only identified functional microbiota in Daqu that affected fermentation quality, but also demonstrated how microorganisms interact to affect the fermentation system, which would provide guidance for microbial supervision in the actual production process. Besides, the application of isothermal microcalorimetry in this study was helpful for us to understand the heat production capacity of microorganisms and their adaptability to the environment. This study presented a commendable framework for improving and controlling the quality of traditional fermentation and inspired further investigations in similar systems.</abstract><cop>United States</cop><pub>American Society for Microbiology</pub><pmid>38506521</pmid><doi>10.1128/aem.01790-23</doi><tpages>21</tpages><orcidid>https://orcid.org/0000-0003-1268-932X</orcidid><orcidid>https://orcid.org/0000-0002-7380-6473</orcidid><orcidid>https://orcid.org/0000-0002-7919-4762</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Bacteria Environmental factors Fermentation Food Microbiology Fungi Heat Heat generation High temperature Metabolism Metabolites Microbiota Microenvironments Microorganisms Next-generation sequencing Pediococcus Solid state fermentation Temperature Yeasts |
title | Pediococcus spp. - mediated competition interaction within Daqu microbiota determines the temperature formation and metabolic profiles |
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