Design of synthetic human gut microbiota ecosystem model for screening potential prebiotics from phytochemicals

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Date

2022

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Sokoine University of Agriculture

Abstract

The human gut microbiota (GM) is a complex and diverse microbial population that is integral to health maintenance. Mechanistic studies of human GM are limited due to its complexity with of over 1,000 species of microorganisms. In this regard, synthetic microbial communities with reduced complexity could be an alternative for GM studies. The main objective of this study was to establish synthetic gut microbial communities for screening of phytochemicals beneficial to gut flora important in the discovery of novel GM therapies. Specifically, this study sought to: (i) investigate conditions for establishment of synthetic gut microbial ecosystem, (ii) determine whether synthetic gut microbial ecosystems can demonstrate prebiotic nature of phytochemicals, and lastly (iii) validate synthetic in vitro gut microbial communities with an in vivo mice study. Firstly, GM key stone species were obtained from Korean Collection for Type Cultures (KCTC) and American Type Culture Collection (ATCC). Next, a suitable medium for re-creation of synthetic microbial communities was sought amongst Chopped Meat Carbohydrate (CMC), Bryant and Burkey (BB), Tryptic Soy Agar (TSA), Brain Heart Infusion (BHI), Reinforced Clostridium Medium (RCM), and Gifu Anaerobic Medium (GAM). Majority of bacteria could grow well in GAM, and therefore GAM medium was selected for this study. Mucin glycans were supplemented in GAM at 2g/L or 4g/L then investigated if they could simulate synthetic GM ecosystem. Specific genera like Bacteroides, Akkermansia, and Clostridium grew significantly faster in mucin-supplemented GAM (p< 0.05, n=3). The synthetic gut microbial community were then assembled and co-cultured in mucin supplemented GAM followed by microbial community profiling and short-chain fatty acids quantitation. Co- culture results showed that mucin stimulated beneficial bacteria such as Collinsella, Bifidobacterium, Ruminococcus, and Lactobacillus compared to gut opportunistic pathogens like Escherichia. Nevertheless, acetate proportion was higher in the mucin-supplemented consortia (p < 0.05, p < 0.001, n=9) and this was highly related with microbial composition in this group. However, some bacteria were not represented in this set-up and this could be attributed to the lack of a real mucosal layer that could be a niche and also a carbon source for bacteria. In this regard, mucosal layer was incorporated using mucin agar-gel. Upon analysis, specific bacterial genera like Roseburia, Bifidobacterium, Lactobacillus, and Collinsella were able to colonize well in the solid mucin-agar component, while Enterococcus, Veilonella, and Clostridium dominated in the liquid part (p < 0.05, p< 0.01, n=5). Metabolic functional prediction in the two experimental setups showed that predicted functional pathways were highly related to microbial composition. The second study applied synthetic microbial communities cultivated in a mucosal simulated environment to test effects of anthraquinone (phytochemical) on top essential gut bacteria. A growing body of research shows that phytochemicals in plants can affect the composition of the GM. As a result, the GM is a good candidate for nutritional interventions aimed at improving health. The anthraquinones examined in this study include emodin, obtusifolin, obtusin, aurantio- obtusin, chryso-obtusin, Gluco-aurantio-obtusin, and Gluco-obtusifolin. Single bacterial isolates were cultivated with these compounds at 100 mM and growth was measured at OD 600 for 18 to 24 h at 37 °C. Results showed emodin to stimulate beneficial bacteria including Akkermansia, Clostridium, Roseburia, and Ruminococcus but inhibited major gut enterotypes (Bacteroides and Prevotella) which are associated with gut inflammation. Emodin also preserved high levels of beneficial anti-inflammatory gut bacteria isolates such as Roseburia and Faecalibacterium while again inhibiting Bacteroides and Prevotella in co- cultivation. To validate the synthetic microbial communities’ co-cultivation and its application in GM-phytochemicals studies, an in vivo study was performed. Mice were randomly divided into three groups: normal group, low emodin (10 mg·kg -1 ) group, and high emodin (50 mg·kg -1 ) group. Emodin was administered by oral gavage for one week followed by sample harvesting and microbial community profiling. Emodin stimulated the anti-inflammatory bacteria Roseburia in co-culture as in mono-culture and Faecalibacterium in co-culture, these bacteria were not detected in vivo, but emodin stimulated Clostridium and Ruminococcus in vivo (which are related to Roseburia and Faecalibacterium). Nevertheless, emodin also induced anti-inflammatory immune cells, which may correlate with its impact on specific gut bacteria in vivo. Gut ecosystem simulation is an advance to mechanically understand the role of the GM in health and diseases necessary in developing innovative GM-phytochemicals therapies. In conclusion, this study has demonstrated that single bacteria culture, synthetic gut ecosystem and in vivo mice experiment can be used for diverse microbiome research since they showed consistent results for major GM changes. I recommend use of synthetic GM ecosystem model in rapid identification of phytochemicals of therapeutic significance.

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Keywords

Human gut, Microbiota, Potential prebiot, Phytochemicals, Microbial ecosystem

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