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Influence of Diet on the Gut Microbiome and Implications for Human Health

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Influence of Diet on the Gut Microbiome and Implications for Human Health Singh et al. J Transl Med (2017) 15:73 DOI 10.1186/s12967-017-1175-y Journal of Translational Medicine REVIEW Open Access Infuence of diet on the gut microbiome and implications for human health Rasnik K. Singh1, Hsin‑Wen Chang2, Di Yan2, Kristina M. Lee2, Derya Ucmak2, Kirsten Wong2, Michael Abrouk3, Benjamin Farahnik4, Mio Nakamura2, Tian Hao Zhu5, Tina Bhutani2 and Wilson Liao2* Abstract Recent studies have suggested that the intestinal microbiome plays an important role in modulating risk of several chronic diseases, including infammatory bowel disease, obesity, type 2 diabetes, cardiovascular disease, and cancer. At the same time, it is now understood that diet plays a signifcant role in shaping the microbiome, with experiments showing that dietary alterations can induce large, temporary microbial shifts within 24 h. Given this association, there may be signifcant therapeutic utility in altering microbial composition through diet. This review systematically evaluates current data regarding the efects of several common dietary components on intestinal microbiota. We show that consumption of particular types of food produces predictable shifts in existing host bacterial genera. Fur‑ thermore, the identity of these bacteria afects host immune and metabolic parameters, with broad implications for human health. Familiarity with these associations will be of tremendous use to the practitioner as well as the patient. Keywords: Diet, Health, Metabolism, Microbiome, Microbiota, Nutrition Background in the distal gut contribute to host health through bio- The gut microbiome synthesis of vitamins and essential amino acids, as well Te human gut microbiome encompasses 10­ 14 resident as generation of important metabolic byproducts from microorganisms, including bacteria, viruses, fungi, and dietary components left undigested by the small intes- protozoa, that are commensal with the human intestinal tine [7]. Short chain fatty acid (SCFA) byproducts such tract [1]. Among these, bacteria represent the most well as butyrate, propionate, and acetate act as a major energy studied group and will be the main focus of this review. source for intestinal epithelial cells and may therefore Overall the predominant bacterial groups in the micro- strengthen the mucosal barrier [8]. Additionally, studies biome are gram positive Firmicutes and gram negative conducted using germ-free mice suggest that the micro- Bacteroidetes [2, 3]. Recently, it has been shown that biota directly promote local intestinal immunity through microbiota can efectively be subdivided into diferent their efects on toll-like receptor (TLR) expression [9], enterotypes, each enriched by particular bacterial genera, antigen presenting cells, diferentiated T cells, and lym- but that all seem to share high functional uniformity [4]. phoid follicles [10, 11], as well as by afecting systemic Tis uniformity exists regardless of several host proper- immunity through increased splenic ­CD4+ T cells and ties, such as age, sex, body mass index, and nationality systemic antibody expression [12]. [5]. Tese recorded benefts and more have led to growing Te majority of microorganisms reside within the interest in the ability to modify the gut microbiota. An more distal parts of the digestive tract, where their bio- acute change in diet—for instance to one that is strictly mass surpasses ­1011 cells per gram content [6]. Microbes animal-based or plant-based—alters microbial com- position within just 24 h of initiation, with reversion to baseline within 48 h of diet discontinuation [13]. Fur- *Correspondence: [email protected] 2 Department of Dermatology, University of California, San Francisco, thermore, the gut microbiome of animals fed a high-fat 2340 Sutter St. Room N431, Box 0808, San Francisco, CA 94115, USA or high-sugar diet is more prone to circadian rhythm Full list of author information is available at the end of the article disruption [14]. Studies also suggest that overwhelming © The Author(s) 2017. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Singh et al. J Transl Med (2017) 15:73 Page 2 of 17 systemic stress and infammation—such as that induced and phosphatidylcholine that produces the proathero- via severe burn injury—can also produce characteristic genic compound, trimethylamine-N-oxide (TMAO) [24]. acute changes in the gut microbiota within just one day A recent study also demonstrated that gut bacteria can of the sustained insult [15]. produce signifcant amounts of amyloid and lipopolysac- charides, which are key players in the pathogenesis of The microbiome in disease Alzheimer’s disease [25]. Tese observations illustrate the Studies examining the composition and role of the important role of microorganisms in human health and intestinal microbiome in diferent disease states have suggest that manipulating them may infuence disease uncovered associations with infammatory bowel dis- activity. While the microbiome of a healthy individual is eases (IBD), infammatory skin diseases such as psoria- relatively stable, gut microbial dynamics can certainly be sis and atopic dermatitis, autoimmune arthritis, type 2 infuenced by host lifestyle and dietary choices [26]. diabetes, obesity, and atherosclerosis. For instance, IBD In this review, we comprehensively explore the ability patients tend to have less bacterial diversity as well as of the host diet to modulate gut bacteria, with the hope lower numbers of Bacteroides and Firmicutes—which that this knowledge will guide our understanding of how together may contribute to reduced concentrations of dietary choices impact human health through alteration microbial-derived butyrate. Butyrate and other SCFAs of the gastrointestinal ecosystem (Fig. 1, Table 1). are thought to have a direct anti-infammatory efect in the gut [16]. Furthermore, diferent indices of Crohn’s Methods disease activity have each been characterized by specifc We performed a systematic literature review in Septem- gut mucosa-attached bacteria, that in turn are signif- ber 2015 by searching the electronic MEDLINE database cantly infuenced by anti-TNF therapy [17]. Te relative via PubMed. Search terms included combinations of the abundance of diferent bacteria may mediate intesti- terms “microbiota”, “intestinal mucosa/microbiology”, nal infammation and Crohn’s disease activity through “gastrointestinal tract/microbiology”, “gastrointestinal efects on local regulatory T cell populations [17, 18]. diseases/microbiology”, with “diet”, “food”, “polysaccha- Furthermore, overrepresentation analysis has shown that rides”, “carbohydrates”, “proteins”, “meat”, “fat”, “lactose”, enzymes enriched in IBD microbiomes are more fre- “oligofructose”, “prebiotics”, “probiotics”, “polyphenols”, quently involved in membrane transport, which could “starch”, “soy”, “sucrose”, “fructose”, “diet, vegetarian”, support a “leaky gut hypothesis” contributing to the “diet, western”, “cereals”, “dietary fber”, and “dietary sup- disease state [19, 20]. Interestingly, autoimmune T17 plements”. Articles were reviewed independently by diferentiation from naïve T cells appears to be depend- two investigators, R.K.S. and K.M.L, and this was adju- ent on the segmented flamentous bacteria. Studies have dicated by W.L. We limited our search to articles avail- shown that T17 cells are absent in the small-intestinal able in English, human studies, and those published lamina propria of germ-free animals, which is the major between 1970 and 2015. We excluded studies that did not site of their diferentiation. Furthermore, introduction explicitly address the efect of a dietary intervention on of segmented flamentous bacteria is sufcient to trig- microbial composition. Manual searches through refer- ger autoimmune arthritis in these animals through pro- ence lists of the articles were also performed to identify motion of T17 cell development in the lamina propria additional studies. Tis resulted in a total of 188 arti- and spleen [20, 21]. Te gut microbiota of patients with cles being selected for inclusion in this review. Studies type 2 diabetes has been functionally characterized with describing the relationship between specifc dietary com- diabetes-associated markers, showing enriched mem- ponents and intestinal microbiota composition ranged brane transport of sugars and branched-chain amino from subject number n = 3 to n = 344, with a majority acids, xenobiotic metabolism, and sulphate reduction of studies clustered around subject number n = 20 to along with decreased bacterial chemotaxis, butyrate syn- 70. Study designs were primarily randomized controlled thesis and metabolism of cofactors and vitamins [22]. trials, cross-sectional studies, case–control studies, and Obesity has been characterized by an altered intestinal in vitro studies. In addition to human studies, several Bacteroides:Firmicutes ratio, with greater relative abun- animal studies were also included to demonstrate dietary dance of Firmicutes. Furthermore, studies involving impact on the microbiome under controlled
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