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Consumption of a Leuconostoc Holzapfelii-Enriched Synbiotic Yang et al. Experimental & Molecular Medicine (2019) 51:87 https://doi.org/10.1038/s12276-019-0288-1 Experimental & Molecular Medicine ARTICLE Open Access Consumption of a Leuconostoc holzapfelii- enriched synbiotic beverage alters the composition of the microbiota and microbial extracellular vesicles Jinho Yang1,2, Andrea McDowell1, Eun Kyoung Kim1, Hochan Seo1, Kyujin Yum3,WonHeeLee1, Young-Koo Jee 4 and Yoon-Keun Kim1 Abstract Synbiotics, the combination of probiotics and prebiotics, are known to confer health benefits via intestinal microbiota modulation. However, significant intestinal microbiota alterations can be difficult to determine in intervention studies based on solely bacterial stool metagenomic analysis. Intestinal microbiota constituents secrete 20–200-nm-sized extracellular vesicles (EVs) containing microbial DNA, proteins, and lipids that are distributed throughout the body, providing an alternative target for microbiota metagenomic analysis. Here, we determined the impact of a synbiotic beverage enriched with the kimchi-derived bacterium Leuconostoc holzapfelii (L. holzapfelii) on the intestinal microbiota and local and circulatory microbiota-derived EV composition of healthy Korean adults. We isolated microbial DNA from stool bacteria, stool EVs, and urinary EVs and conducted next-generation sequencing of the 16S rDNA V3–V4 regions before and after synbiotic consumption. The species diversity of circulating urinary EVs was 1234567890():,; 1234567890():,; 1234567890():,; 1234567890():,; significantly increased after synbiotic consumption, while stool bacterial and EV diversity remained unchanged. Furthermore, we found that while a single genus was decreased among the stool bacteria constituents, stool EVs and urinary EVs showed significant alterations in four and eight genera, respectively. Blood chemistry assays revealed that synbiotic consumption significantly lowered aspartate aminotransferase (AST) serum levels, particularly in subjects with starting levels above the normal range (>40 UI/L). In conclusion, the L. holzapfelii-enriched synbiotic beverage greatly altered serum AST levels and microbial EV composition in urine and stool, while only minor changes were observed in the gut microbiota composition. Based on these findings, we suggest the potential use of microbiota-derived EVs as surrogate markers in future predictive diagnosis studies. Introduction with the host and has essential roles in host immunity, The gut microbiota is a community of trillions of bac- metabolism, and nutrition3. To foster a healthy gut teria residing in the intestinal tract, which is comprised of microbiota balance, regular consumption of beneficial ~2000 species that contribute over two million genes to probiotic bacteria is highly recommended. Probiotics are the host1,2. This complex ecosystem exists symbiotically living microorganisms that confer beneficial health effects by modulating the gut microbiota when consumed in sufficient amounts. Probiotic consumption has been Correspondence: Yoon-Keun Kim ([email protected]) or Young-Koo Jee ([email protected]) shown to have therapeutic and prophylactic effects in a 1MD Healthcare Inc., Seoul, Republic of Korea wide array of gastrointestinal diseases and immune dis- 2 Department of Health and Safety Convergence Science, Korea University, orders associated with gut microbiota dysbiosis4,5. Seoul, Republic of Korea Full list of author information is available at the end of the article. Although the health benefits of probiotics have been These authors contributed equally: Jinho Yang, Andrea McDowell © The Author(s) 2019 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 linktotheCreativeCommons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license 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 license, visit http://creativecommons.org/licenses/by/4.0/. Official journal of the Korean Society for Biochemistry and Molecular Biology Yang et al. Experimental & Molecular Medicine (2019) 51:87 Page 2 of 11 recognized for centuries, recent interest has shifted significant changes in the gut microbiota composition in toward the optimization of probiotic efficacy. A common response to particular probiotic or synbiotic treatments. strategy to increase the probiotic effect is the inclusion of Therefore, recent efforts have focused on characterizing prebiotics, nondigestible dietary components that benefit changes in the functional activities of the microbiome as the host through promotion of selective bacterial growth well as compositional alterations. To decipher the com- in the intestinal tract. Synbiotics, the combination of plex, systemic network of interactions between the gut probiotics and prebiotics, are a promising advancement in microbiota and human host, recent studies have investi- the field of functional foods, as conventional probiotics gated the role of microbial-derived extracellular vesicles alone have limited implantation and survival in the gas- (EVs) in host health19,20. Bacterial EVs are ubiquitously trointestinal tract without the aid of prebiotics6,7. released nanovesicles 20–200 nm in diameter that distally Optimally synergistic probiotic bacterial strains and transport bacterial proteins, nucleic acids, lipids, and prebiotics must be selected to develop synbiotic for- other components to host and bacterial cells throughout mulations with maximal health benefits. Effective pro- the body21. In addition to their functional properties in biotic bacteria are often isolated from fermented foods. the host, the inclusion of bacterial DNA enables meta- Kimchi is a traditional Korean fermented food known to genomic analysis of 16S rDNA contained in bacterial EVs, have health-promoting activity because it serves as a rich allowing the identification and characterization of bac- source of probiotic bacteria. Kimchi contains a variety of terial EV activity both locally and systemically. lactic acid bacteria (LAB) that have been shown to have As the probiotic potential of LAB isolated from fer- antioxidant, immunomodulatory, and antiadipogenic mented foods has become increasingly recognized, it is activities8. Several species belonging to the genera Leu- necessary to understand how the microbiota composition conostoc are LAB commonly found in kimchi and have and activity changes in response to the consumption of been previously used as probiotics in a variety of appli- specific strains and synbiotic formulations. In this study, cations, such as silage and prevention of oral biofilm we conducted a clinical trial in which participants con- formation9,10. Leuconostoc holzapfelii (L. holzapfelii)is sumed a synbiotic beverage including L. holzapfelii iso- one species commonly isolated from kimchi that hetero- lated from kimchi and prebiotics such as black soybean, fermentatively produces lactic acid and mannitol, a polyol broccoli, fo-ti, and persimmon vinegar for 4 weeks. Then, with beneficial health effects as an antioxidant and non- 16S rDNA metagenomic analysis was conducted on bac- metabolizable sugar11. However, to our knowledge, the teria isolated from stool as well as microbiota-derived EVs effects of L. holzapfelii consumption on the gut micro- isolated from stool and urine to assess holistic micro- biota composition and blood chemistry of healthy human biome changes before and after consumption of the L. subjects have yet to be published. Selection of prebiotics holzapfelii-enriched synbiotic beverage. In addition, a with high oligosaccharide content and other beneficial wide array of blood chemistry assays were performed to characteristics, such as antioxidant activity, is also critical screen for potential blood chemistry alterations induced for optimal synbiotic development. Dietary fibers rich in by the synbiotic intervention. oligosaccharides are indigestible in the small intestine and pass to the colon, where they are fermented by com- Materials and methods mensal gut bacteria. Oligosaccharide fermentation has a Subjects myriad of beneficial effects, including acidification of the In total, 21 healthy people, 9 males and 12 females, were colon, increased populations of Lactobacilli and Bifido- enrolled from Dankook University Hospital in 2017. bacteria, increased production of short-chain fatty acids, Exclusion criteria included being under 20 years old, and increased colon crypt depth12,13. Soybeans and having cancer or diabetes, being pregnant, taking medi- broccoli are rich sources of indigestible, fermentable oli- cation, and participating in another clinical trial. The gosaccharides, making them ideal prebiotics14. In addi- present study was approved by the Institutional Review tion, food ingredients high in polyphenols and vitamins, Board of Dankook University Hospital (IRB No. DKUH such as broccoli, black soybeans, persimmon oil, and fo-ti, 2017–05–020). The methods conducted in this study have high antioxidant activity, further contributing to were in accordance with the approved
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