Temperature-Induced Annual Variation in Microbial Community Changes and Resulting Metabolome Shifts in a Controlled Fermentation System

ABSTRACT We are rapidly increasing our understanding on the spatial distribution of microbial communities. However, microbial functioning, as well as temporal differences and mechanisms causing microbial community shifts, remains comparably little explored. Here, using Chinese liquor fermentation as...

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Autores principales:	Shilei Wang, Wu Xiong, Yuqiao Wang, Yao Nie, Qun Wu, Yan Xu, Stefan Geisen
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	fermentation system microbiome seasonal factors temperature-induced Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/cd194240b90e4d7695686138c83cdcab
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spelling	oai:doaj.org-article:cd194240b90e4d7695686138c83cdcab2021-12-02T18:23:16ZTemperature-Induced Annual Variation in Microbial Community Changes and Resulting Metabolome Shifts in a Controlled Fermentation System10.1128/mSystems.00555-202379-5077https://doaj.org/article/cd194240b90e4d7695686138c83cdcab2020-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00555-20https://doaj.org/toc/2379-5077ABSTRACT We are rapidly increasing our understanding on the spatial distribution of microbial communities. However, microbial functioning, as well as temporal differences and mechanisms causing microbial community shifts, remains comparably little explored. Here, using Chinese liquor fermentation as a model system containing a low microbial diversity, we studied temporal changes in microbial community structure and functioning. For that, we used high-throughput sequencing to analyze the composition of bacteria and fungi and analyzed the microbially derived metabolome throughout the fermentation process in all four seasons in both 2018 and 2019. We show that microbial communities and the metabolome changed throughout the fermentation process in each of the four seasons, with metabolome diversity increasing throughout the fermentation process. Across seasons, bacterial and fungal communities as well as the metabolome driven by 10 indicator microorganisms and six metabolites varied even more. Daily average temperature in the external surroundings was the primary determinant of the observed temporal microbial community and metabolome changes. Collectively, our work reveals critical insights into patterns and processes determining temporal changes of microbial community composition and functioning. We highlight the importance of linking taxonomic to functional changes in microbial ecology to enable predictions of human-relevant applications. IMPORTANCE We used Chinese liquor fermentation as a model system to show that microbiome composition changes more dramatically across seasons than throughout the fermentation process within seasons. These changes translate to differences in the metabolome as the ultimate functional outcome of microbial activity, suggesting that temporal changes in microbiome composition are translating into functional changes. This result is striking as it suggests that microbial functioning, despite controlled conditions in the fermentors, fluctuates over season along with external temperature differences, which threatens a reproducible food taste. As such, we believe that our study provides a stepping-stone into novel taxonomy-functional studies that promote future work in other systems and that also is relevant in applied settings to better control surrounding conditions in food production.Shilei WangWu XiongYuqiao WangYao NieQun WuYan XuStefan GeisenAmerican Society for Microbiologyarticlefermentation systemmicrobiomeseasonal factorstemperature-inducedMicrobiologyQR1-502ENmSystems, Vol 5, Iss 4 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	fermentation system microbiome seasonal factors temperature-induced Microbiology QR1-502
spellingShingle	fermentation system microbiome seasonal factors temperature-induced Microbiology QR1-502 Shilei Wang Wu Xiong Yuqiao Wang Yao Nie Qun Wu Yan Xu Stefan Geisen Temperature-Induced Annual Variation in Microbial Community Changes and Resulting Metabolome Shifts in a Controlled Fermentation System
description	ABSTRACT We are rapidly increasing our understanding on the spatial distribution of microbial communities. However, microbial functioning, as well as temporal differences and mechanisms causing microbial community shifts, remains comparably little explored. Here, using Chinese liquor fermentation as a model system containing a low microbial diversity, we studied temporal changes in microbial community structure and functioning. For that, we used high-throughput sequencing to analyze the composition of bacteria and fungi and analyzed the microbially derived metabolome throughout the fermentation process in all four seasons in both 2018 and 2019. We show that microbial communities and the metabolome changed throughout the fermentation process in each of the four seasons, with metabolome diversity increasing throughout the fermentation process. Across seasons, bacterial and fungal communities as well as the metabolome driven by 10 indicator microorganisms and six metabolites varied even more. Daily average temperature in the external surroundings was the primary determinant of the observed temporal microbial community and metabolome changes. Collectively, our work reveals critical insights into patterns and processes determining temporal changes of microbial community composition and functioning. We highlight the importance of linking taxonomic to functional changes in microbial ecology to enable predictions of human-relevant applications. IMPORTANCE We used Chinese liquor fermentation as a model system to show that microbiome composition changes more dramatically across seasons than throughout the fermentation process within seasons. These changes translate to differences in the metabolome as the ultimate functional outcome of microbial activity, suggesting that temporal changes in microbiome composition are translating into functional changes. This result is striking as it suggests that microbial functioning, despite controlled conditions in the fermentors, fluctuates over season along with external temperature differences, which threatens a reproducible food taste. As such, we believe that our study provides a stepping-stone into novel taxonomy-functional studies that promote future work in other systems and that also is relevant in applied settings to better control surrounding conditions in food production.
format	article
author	Shilei Wang Wu Xiong Yuqiao Wang Yao Nie Qun Wu Yan Xu Stefan Geisen
author_facet	Shilei Wang Wu Xiong Yuqiao Wang Yao Nie Qun Wu Yan Xu Stefan Geisen
author_sort	Shilei Wang
title	Temperature-Induced Annual Variation in Microbial Community Changes and Resulting Metabolome Shifts in a Controlled Fermentation System
title_short	Temperature-Induced Annual Variation in Microbial Community Changes and Resulting Metabolome Shifts in a Controlled Fermentation System
title_full	Temperature-Induced Annual Variation in Microbial Community Changes and Resulting Metabolome Shifts in a Controlled Fermentation System
title_fullStr	Temperature-Induced Annual Variation in Microbial Community Changes and Resulting Metabolome Shifts in a Controlled Fermentation System
title_full_unstemmed	Temperature-Induced Annual Variation in Microbial Community Changes and Resulting Metabolome Shifts in a Controlled Fermentation System
title_sort	temperature-induced annual variation in microbial community changes and resulting metabolome shifts in a controlled fermentation system
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/cd194240b90e4d7695686138c83cdcab
work_keys_str_mv	AT shileiwang temperatureinducedannualvariationinmicrobialcommunitychangesandresultingmetabolomeshiftsinacontrolledfermentationsystem AT wuxiong temperatureinducedannualvariationinmicrobialcommunitychangesandresultingmetabolomeshiftsinacontrolledfermentationsystem AT yuqiaowang temperatureinducedannualvariationinmicrobialcommunitychangesandresultingmetabolomeshiftsinacontrolledfermentationsystem AT yaonie temperatureinducedannualvariationinmicrobialcommunitychangesandresultingmetabolomeshiftsinacontrolledfermentationsystem AT qunwu temperatureinducedannualvariationinmicrobialcommunitychangesandresultingmetabolomeshiftsinacontrolledfermentationsystem AT yanxu temperatureinducedannualvariationinmicrobialcommunitychangesandresultingmetabolomeshiftsinacontrolledfermentationsystem AT stefangeisen temperatureinducedannualvariationinmicrobialcommunitychangesandresultingmetabolomeshiftsinacontrolledfermentationsystem
_version_	1718378124028149760

Temperature-Induced Annual Variation in Microbial Community Changes and Resulting Metabolome Shifts in a Controlled Fermentation System

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