Critical Reviews in Food Science and Nutrition ISSN: 1040-8398 (Print) 1549-7852 (Online) Journal homepage: https://www.tandfonline.com/loi/bfsn20 Nondigestible carbohydrates, butyrate, and butyrate-producing bacteria Xiaodan Fu, Zhemin Liu, Changliang Zhu, Haijin Mou & Qing Kong To cite this article: Xiaodan Fu, Zhemin Liu, Changliang Zhu, Haijin Mou & Qing Kong (2018): Nondigestible carbohydrates, butyrate, and butyrate-producing bacteria, Critical Reviews in Food Science and Nutrition, DOI: 10.1080/10408398.2018.1542587 To link to this article: https://doi.org/10.1080/10408398.2018.1542587 Published online: 22 Dec 2018. Submit your article to this journal Article views: 112 View Crossmark data Full Terms & Conditions of access and use can be found at https://www.tandfonline.com/action/journalInformation?journalCode=bfsn20 CRITICAL REVIEWS IN FOOD SCIENCE AND NUTRITION https://doi.org/10.1080/10408398.2018.1542587 REVIEW Nondigestible carbohydrates, butyrate, and butyrate-producing bacteria Xiaodan Fu, Zhemin Liu, Changliang Zhu, Haijin Mou, and Qing Kong College of Food Science and Engineering, Ocean University of China, Qingdao, China ABSTRACT KEYWORDS Nondigestible carbohydrates (NDCs) are fermentation substrates in the colon after escaping diges- Nondigestible carbohy- tion in the upper gastrointestinal tract. Among NDCs, resistant starch is not hydrolyzed by pancre- drates; oligosaccharides; atic amylases but can be degraded by enzymes produced by large intestinal bacteria, including short-chain fatty acids; butyrate; butyrate- clostridia, bacteroides, and bifidobacteria. Nonstarch polysaccharides, such as pectin, guar gum, producing bacteria alginate, arabinoxylan, and inulin fructans, and nondigestible oligosaccharides and their deriva- tives, can also be fermented by beneficial bacteria in the large intestine. Butyrate is one of the most important metabolites produced through gastrointestinal microbial fermentation and func- tions as a major energy source for colonocytes by directly affecting the growth and differentiation of colonocytes. Moreover, butyrate has various physiological effects, including enhancement of intestinal barrier function and mucosal immunity. In this review, several representative NDCs are introduced, and their chemical components, structures, and physiological functions, including promotion of the proliferation of butyrate-producing bacteria and enhancement of butyrate production, are discussed. We also describe the strategies for achieving directional accumulation of colonic butyrate based on endogenous generation mechanisms. Introduction shown to play an important role in modulating immune and inflammatory responses and intestinal barrier function Studies on nondigestible carbohydrates (NDCs), including and in preventing colon cancers (Hamer et al. 2008; Elamin undigested plant polysaccharides, resistant starch (RS), and et al. 2013). Furthermore, recent studies have shown that nondigestible oligosaccharides (NDOs), have attracted atten- NDCs consumption and dietary butyrate supplementation tion owing to the functions of these materials as dietary have beneficial effects on health by decreasing adiposity and fibers (DFs) (Mussatto and Mancilha 2007; Smith and improving insulin sensitivity (McNabney and Henagan 2017; Tucker 2011; Holscher 2017). Human enzymes are capable Henagan et al. 2015). of degrading only a few glycosidic linkages present in carbo- In recent years, specific gut microbiota has attracted hydrates; however, intestinal bacteria possess many enzymes, attention owing to their important roles in gut metabolism including glycoside hydrolases, polysaccharide lyases, glyco- and homeostasis. In particularly, butyrogenic bacteria from syltransferases, and carbohydrate esterases, that are necessary within the Firmicutes/Clostridium clusters IV and XIVa have for carbohydrate utilization (Englyst, Hay, and Macfarlane been taken as probiotics to increase colonic butyrate levels 1987; Lombard et al. 2014). Thus, NDCs can escape diges- and optimize gut health (Scott et al. 2014; Hossain, Begum, tion in the host gastrointestinal tract to be metabolized by and Kim 2015). Various strategies are available to enhance the microbiota in the cecum and colon (Ning et al. 2017). butyrate levels in the distal intestine. Supplementation with The metabolism of NDCs generate a variety of products, NDCs, such as RS (Brouns, Kettlitz, and Arrigoni 2002), including short-chain fatty acids (SCFAs; e.g., acetate, propi- psyllium fiber (Marteau et al. 1994), and guar gum (Pylkas, onate, and butyrate), gases (e.g., H2,H2S, CO2, and CH4), Juneja, and Slavin 2005), is another widely recognized and organic acids (e.g., lactate, succinate, and pyruvate), approach. Butyrate production of NDCs can be influenced which affect the host health to different extents (Macfarlane by many factors, such as the solubility, the distribution of and Macfarlane 2012; Koh et al. 2016). chain lengths, branching and substituents, the monomeric SCFAs, primarily acetate, propionate, and butyrate, have carbohydrate composition, and linkage type between mono- been estimated to provide approximately 60–70% of the mers (Karppinen et al. 2000; Henningsson, Bjorck,€ and energy requirements of colonic epithelial cells (Brahe, Nyman 2002; Nilsson and Nyman 2005). Additionally, Astrup, and Larsen 2013). Specifically, the four-carbon cross-feeding interactions between bacteria also affect SCFA butyrate is the major energy source for colonocytes, colonic fermentation through modulating microbial mutual- directly affecting the growth and differentiation of these cells istic symbiosis and competitive fitness (Morrison and (Jacobi and Odle 2012; Chen et al. 2015). Butyrate has been Preston 2016). However, the current understanding on the CONTACT Haijin Mou [email protected]; Qing Kong [email protected] Ocean University of China, College of Food Science and Engineering, No. 5 Yushan Road, Qingdao 266003, Shandong, China. Color versions of one or more of the figures in the article can be found online at www.tandfonline.com/bfsn. ß 2018 Taylor & Francis Group, LLC 2 X. FU ET AL. composition and metabolism of intestinal microbiota is still individual variations in microbiota composition (Karppinen insufficient, which limits the application of this approach. et al. 2000; Henningsson, Bjorck,€ and Nyman 2002;Nilsson In this review, we summarize recent studies on NDCs and Nyman 2005; Louis et al. 2010). Moreover, the gut with butyrogenic effects, factors affecting butyrate produc- bacteria differ in their possession of degradative enzymes and tion, and physiological effects and mechanism of butyrate. transport systems, which likely determines the substrate pref- Based on our analysis, the strategies of combining different erence and competitive ability of a given bacteria, and conse- NDCs and probiotic bacterial strains related with butyrate- quently the butyrate-producing ability (Flint 2004;vander production can be potentially meaningful to achieve direc- Meulen et al. 2006). tional accumulation of colonic butyrate. Previously described butyrate-producing bacteria in the human gastrointestinal intestinal tract are commonly distrib- uted in the phylum Firmicutes and the order Clostridiales Butyrate production and physiological effects (Table. 1). The majority of these producers belong to four fam- Butyrate production from NDCs ilies: Clostridiaceae, Eubacteriaceae, Lachnospiraceae, and Ruminococcaceae; however, not all the members within these The human large intestine contains a very dense microbial families are butyrogenic (Duncan et al. 2002;Louisetal.2004; (>1011 bacteria per gram) community composed largely of a Louis and Flint 2009;Vital,Howe,andTiedje2014). Members metabolically active microbiota (Flint et al. 2007). This com- within other families such as Veillonellaceae (e.g., Megasphaera munity plays an important role in health and largely elsdenii) and Thermoanaerobacterales Family III (e.g., depends on dietary carbohydrate as an energy source. Most Caldocellum saccharolyticum) have also been identified as of these carbohydrates cannot be degraded by the host and butyrate producers (Louis et al. 2004; Tsukahara et al. 2002). are therefore broken down by the gut microbiota owing to Most butyrate producers in the order Clostridiales are widely their more excellent degradative enzymes and metabolic distributed across several clusters including clusters IV, XIVa, capabilities than their hosts (Flint et al. 2008; Kurokawa XVI, and I. Among them, two of the most important groups, et al. 2007). Most of the dietary carbohydrates that reach the F. prausnitzii (clostridial cluster IV) and Eubacterium rectale large intestine are generally insoluble fragments of plant (clostridial cluster XIVa), have been studied extensively because fiber, which largely consists of plant cell-wall polysaccharides they typically constitute up to 12 À 14% of the total gut micro- and starch particles, as well as oligosaccharides and storage polysaccharides (Flint et al. 2008). However, only a few gut biota in fecal samples of healthy adults based on 16S rRNA bacteria are available to degrade the insoluble substrates. gene sequencing (Walker et al., 2014). Moreover, other typical Specialized primary degraders, typically cellulolytic bacteria, butyrogenic species are also widely distributed across cluster are able to release a wider range of solubilized products (e.g. XIVa (e.g., Roseburia spp., Anaerostipes spp., Clostridium spp., polysaccharides and oligosaccharides)