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Ecological Adaptation and Succession of Human Fecal Microbial Communities in an Automated In Vitro Fermentation System.

ABSTRACT: Longitudinal studies of gut microbiota following specific interventions are vital for understanding how they influence host health. However, robust longitudinal sampling of gut microbiota is a major challenge, which can be addressed using in vitro fermentors hosting complex microbial communities. Here, by employing 16S rRNA gene amplicon sequencing, we investigated the adaptation and succession of human fecal microbial communities in an automated multistage fermentor. We performed two independent experiments using different human donor fecal samples, one configured with two units of three colon compartments each studied for 22 days and another with one unit of two colon compartments studied for 31 days. The fermentor maintained a trend of increasing microbial alpha diversity along colon compartments. Within each experiment, microbial compositions followed compartment-specific trajectories and reached independent stable configurations. While compositions were highly similar between replicate units, they were clearly separated between different experiments, showing that they maintained the individuality of fecal inoculum rather than converging on a fermentor-specific composition. While some fecal amplicon sequence variants (ASVs) were undetected in the fermentor, many ASVs undetected in the fecal samples flourished in vitro. These bloomer ASVs accounted for significant proportions of the population and included prominent health-associated microbes such as Bacteroides fragilis and Akkermansia muciniphila. Turnover in community compositions is likely explained by feed composition and pH, suggesting that these communities can be easily modulated. Our results suggest that in vitro fermentors are promising tools to study complex microbial communities harboring important members of human gut microbiota. IMPORTANCE In vitro fermentors that can host complex gut microbial communities are promising tools to investigate the dynamics of human gut microbiota. In this work, using an automated in vitro gut fermentor consisting of different colon compartments, we investigated the adaptation dynamics of two different human fecal microbial communities over 22 and 31 days. By observing the temporal trends of different community members, we found that many dominant members of the fecal microbiota failed to maintain their dominance in vitro, and some of the low-abundance microbes undetected in the fecal microbiota successfully grew in the in vitro communities. Microbiome compositional changes and blooming could largely be explained by feed composition and pH, suggesting that these communities can be modulated to desired compositions via optimizing culture conditions. Thus, our results open up the possibility of modulating in vitro microbial communities to predefined compositions by optimizing feed composition and culture conditions.

SUBMITTER: Gnanasekaran T

PROVIDER: S-EPMC8409738 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Longitudinal studies of gut microbiota following specific interventions are vital for understanding how they influence host health. However, robust longitudinal sampling of gut microbial communities is a major challenge, which can be addressed using in vitro fermenters hosting complex microbial communities. Here, by employing 16S rRNA gene amplicon sequencing, we investigated the adaptation and succession of human fecal microbial communities in an automated in vitro fermenter. We performed two independent experiments each using a different human donor fecal sample – the first experiment was configured with two units of three colon compartments each studied for 22 days, and the second experiment with one unit of two colon compartments studied for 31 days. In both experiments, the fermenter maintained a trend of increasing microbial alpha-diversity along colon compartments, mimicking that of the human gastrointestinal tract. Within each experiment, microbial compositions followed compartment-specific trajectories over time and reached compartment-specific stable configurations. Microbial compositions were highly similar between the replicate units in the first experiment, thus showing reproducibility. Yet, microbial compositions and their trajectories were clearly separated between the two experiments, showing that these in vitro communities maintained the individuality of fecal inocula rather than converging on a fermenter-specific composition. Using longitudinal relative abundance profiles, we identified different dynamics exhibited by individual amplicon sequence variants (ASVs). While we could not detect some fecal ASVs in the in vitro communities, we observed that many ASVs undetected in the fecal sample flourished under in vitro conditions, which we named bloomers. In both experiments, bloomer ASVs accounted for significant proportions of ASV relative abundance after stabilization – 69% and 43% in the descending compartments in the two experiments. Bloomer ASVs included clinically relevant microbes associated with human health such as Bacteroides fragilis and Akkermansia muciniphila. This turnover in community compositions is likely explained by feed composition and pH, suggesting that these communities can be modulated. We characterized the exometabolites in the first experiment, derived a microbe-exometabolite bipartite network for its descending colon compartment, and identified 6 coherent groups based on the exometabolites. Our results suggest that in vitro fermenters are promising tools to study complex microbial communities harboring important members of human gut microbiota.

Project description:Although the importance of microbiota in the natural environment and in industrial production has been widely recognized, little is known about the formation and succession patterns of the microbial community, particularly secondary succession after disturbance. Here, we choose the Xiaoqu liquor brewing process as an experimental model in which sorghum grains were first aerobically saccharified and then anaerobically fermented after being stirred and acidified to explore multistage community succession patterns. We analyzed microbial composition, physicochemical factors, and metabolites of brewing grains inoculated with two different starters, pure starter and traditional starter, respectively. Two groups showed similar succession patterns where the saccharification microbiota was mainly derived from starters, while environmental microorganisms, mainly Lactobacillaceae and Saccharomyces, dominated the fermentation microbiota regardless of the original saccharification community composition. Species replacement shaped the bacterial community, while species replacement and loss both contributed to fungal community succession in both groups. Grain acidification and hypoxia led to the succession of bacterial and fungal communities during fermentation, respectively. Despite inoculation with starters containing different microorganisms, similar microbial communities during the fermentation stage of the two groups exhibited similar metabolite composition. However, higher abundance of Rhizopus in the saccharification of the pure starter group led to more alcohols, while higher abundance of Monascus and Saccharomycopsis in the traditional starter group promoted acid and ester metabolism. These results revealed the microbial succession patterns of two-stage liquor brewing and its influence on flavor metabolism, which could be used to regulate the microbial community in food fermentation to further promote the modernization of the fermented food industry. IMPORTANCE Revealing formation and assembly mechanisms of microbiota can help us to understand and further regulate its roles in the ecosystems. The Xiaoqu liquor brewing system is a tractable microbial ecosystem with low complexity. This two-stage microbial ecosystem can be used as an experimental model to analyze the multistage temporal succession pattern of microbial communities. Our results demonstrated the dynamic composition and succession pattern of a microbial community in the two-stage liquor brewing system. The results also revealed the microbial origins determining community composition, the ecological processes dominating microbial community succession patterns, the determinants affecting microbial community successions, and the effect of microbial community changes on metabolite synthesis. Overall, our study not only provides an insight into multistage succession patterns of microbial communities in liquor brewing systems but also provides reference for optimizing the quality of fermented products, which will be helpful to understand the succession patterns of microbial communities in other natural ecosystems.

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Ecological Adaptation and Succession of Human Fecal Microbial Communities in an Automated In Vitro Fermentation System.

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