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Bacterial quorum sensing orchestrates longitudinal interactions to shape microbiota assembly
BACKGROUND: The mechanism of microbiota assembly is one of the main problems in microbiome research, which is also the primary theoretical basis for precise manipulation of microbial communities. Bacterial quorum sensing (QS), as the most common means for bacteria to exchange information and interac...
Autores principales: | , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10626739/ https://www.ncbi.nlm.nih.gov/pubmed/37926838 http://dx.doi.org/10.1186/s40168-023-01699-4 |
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author | Su, Ying Xu, Ming-ying Cui, Ying Chen, Run-zhi Xie, Li-xiang Zhang, Jing-xiang Chen, Yong-qiu Ding, Tao |
author_facet | Su, Ying Xu, Ming-ying Cui, Ying Chen, Run-zhi Xie, Li-xiang Zhang, Jing-xiang Chen, Yong-qiu Ding, Tao |
author_sort | Su, Ying |
collection | PubMed |
description | BACKGROUND: The mechanism of microbiota assembly is one of the main problems in microbiome research, which is also the primary theoretical basis for precise manipulation of microbial communities. Bacterial quorum sensing (QS), as the most common means for bacteria to exchange information and interactions, is characterized by universality, specificity, and regulatory power, which therefore may influence the assembly processes of human microbiota. However, the regulating role of QS in microbiota assembly is rarely reported. In this study, we developed an optimized in vitro oral biofilm microbiota assembling (OBMA) model to simulate the time-series assembly of oral biofilm microbiota (OBM), by which to excavate the QS network and its regulating power in the process. RESULTS: By using the optimized OBMA model, we were able to restore the assembly process of OBM and generate time-series OBM metagenomes of each day. We discovered a total of 2291 QS protein homologues related to 21 QS pathways. Most of these pathways were newly reported and sequentially enriched during OBM assembling. These QS pathways formed a comprehensive longitudinal QS network that included successively enriched QS hubs, such as Streptococcus, Veillonella-Megasphaera group, and Prevotella-Fusobacteria group, for information delivery. Bidirectional cross-talk among the QS hubs was found to play critical role in the directional turnover of microbiota structure, which in turn, influenced the assembly process. Subsequent QS-interfering experiments accurately predicted and experimentally verified the directional shaping power of the longitudinal QS network in the assembly process. As a result, the QS-interfered OBM exhibited delayed and fragile maturity with prolonged membership of Streptococcus and impeded membership of Prevotella and Fusobacterium. CONCLUSION: Our results revealed an unprecedented longitudinal QS network during OBM assembly and experimentally verified its power in predicting and manipulating the assembling process. Our work provides a new perspective to uncover underlying mechanism in natural complex microbiota assembling and a theoretical basis for ultimately precisely manipulating human microbiota through intervention in the QS network. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-023-01699-4. |
format | Online Article Text |
id | pubmed-10626739 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-106267392023-11-07 Bacterial quorum sensing orchestrates longitudinal interactions to shape microbiota assembly Su, Ying Xu, Ming-ying Cui, Ying Chen, Run-zhi Xie, Li-xiang Zhang, Jing-xiang Chen, Yong-qiu Ding, Tao Microbiome Research BACKGROUND: The mechanism of microbiota assembly is one of the main problems in microbiome research, which is also the primary theoretical basis for precise manipulation of microbial communities. Bacterial quorum sensing (QS), as the most common means for bacteria to exchange information and interactions, is characterized by universality, specificity, and regulatory power, which therefore may influence the assembly processes of human microbiota. However, the regulating role of QS in microbiota assembly is rarely reported. In this study, we developed an optimized in vitro oral biofilm microbiota assembling (OBMA) model to simulate the time-series assembly of oral biofilm microbiota (OBM), by which to excavate the QS network and its regulating power in the process. RESULTS: By using the optimized OBMA model, we were able to restore the assembly process of OBM and generate time-series OBM metagenomes of each day. We discovered a total of 2291 QS protein homologues related to 21 QS pathways. Most of these pathways were newly reported and sequentially enriched during OBM assembling. These QS pathways formed a comprehensive longitudinal QS network that included successively enriched QS hubs, such as Streptococcus, Veillonella-Megasphaera group, and Prevotella-Fusobacteria group, for information delivery. Bidirectional cross-talk among the QS hubs was found to play critical role in the directional turnover of microbiota structure, which in turn, influenced the assembly process. Subsequent QS-interfering experiments accurately predicted and experimentally verified the directional shaping power of the longitudinal QS network in the assembly process. As a result, the QS-interfered OBM exhibited delayed and fragile maturity with prolonged membership of Streptococcus and impeded membership of Prevotella and Fusobacterium. CONCLUSION: Our results revealed an unprecedented longitudinal QS network during OBM assembly and experimentally verified its power in predicting and manipulating the assembling process. Our work provides a new perspective to uncover underlying mechanism in natural complex microbiota assembling and a theoretical basis for ultimately precisely manipulating human microbiota through intervention in the QS network. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-023-01699-4. BioMed Central 2023-11-06 /pmc/articles/PMC10626739/ /pubmed/37926838 http://dx.doi.org/10.1186/s40168-023-01699-4 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data. |
spellingShingle | Research Su, Ying Xu, Ming-ying Cui, Ying Chen, Run-zhi Xie, Li-xiang Zhang, Jing-xiang Chen, Yong-qiu Ding, Tao Bacterial quorum sensing orchestrates longitudinal interactions to shape microbiota assembly |
title | Bacterial quorum sensing orchestrates longitudinal interactions to shape microbiota assembly |
title_full | Bacterial quorum sensing orchestrates longitudinal interactions to shape microbiota assembly |
title_fullStr | Bacterial quorum sensing orchestrates longitudinal interactions to shape microbiota assembly |
title_full_unstemmed | Bacterial quorum sensing orchestrates longitudinal interactions to shape microbiota assembly |
title_short | Bacterial quorum sensing orchestrates longitudinal interactions to shape microbiota assembly |
title_sort | bacterial quorum sensing orchestrates longitudinal interactions to shape microbiota assembly |
topic | Research |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10626739/ https://www.ncbi.nlm.nih.gov/pubmed/37926838 http://dx.doi.org/10.1186/s40168-023-01699-4 |
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