Influence of diet on the gut microbiome and implications for human health
© The Author(s) 2017
Received: 30 September 2016
Accepted: 21 March 2017
Published: 8 April 2017
Recent studies have suggested that the intestinal microbiome plays an important role in modulating risk of several chronic diseases, including inflammatory bowel disease, obesity, type 2 diabetes, cardiovascular disease, and cancer. At the same time, it is now understood that diet plays a significant 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 significant therapeutic utility in altering microbial composition through diet. This review systematically evaluates current data regarding the effects 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. Furthermore, the identity of these bacteria affects 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.
KeywordsDiet Health Metabolism Microbiome Microbiota Nutrition
The gut microbiome
The human gut microbiome encompasses 1014 resident microorganisms, including bacteria, viruses, fungi, and protozoa, that are commensal with the human intestinal tract . Among these, bacteria represent the most well studied group and will be the main focus of this review. Overall the predominant bacterial groups in the microbiome are gram positive Firmicutes and gram negative Bacteroidetes [2, 3]. Recently, it has been shown that microbiota can effectively be subdivided into different enterotypes, each enriched by particular bacterial genera, but that all seem to share high functional uniformity . This uniformity exists regardless of several host properties, such as age, sex, body mass index, and nationality .
The majority of microorganisms reside within the more distal parts of the digestive tract, where their biomass surpasses 1011 cells per gram content . Microbes in the distal gut contribute to host health through biosynthesis of vitamins and essential amino acids, as well as generation of important metabolic byproducts from dietary components left undigested by the small intestine . Short chain fatty acid (SCFA) byproducts such as butyrate, propionate, and acetate act as a major energy source for intestinal epithelial cells and may therefore strengthen the mucosal barrier . Additionally, studies conducted using germ-free mice suggest that the microbiota directly promote local intestinal immunity through their effects on toll-like receptor (TLR) expression , antigen presenting cells, differentiated T cells, and lymphoid follicles [10, 11], as well as by affecting systemic immunity through increased splenic CD4+ T cells and systemic antibody expression .
These recorded benefits and more have led to growing interest in the ability to modify the gut microbiota. An acute change in diet—for instance to one that is strictly animal-based or plant-based—alters microbial composition within just 24 h of initiation, with reversion to baseline within 48 h of diet discontinuation . Furthermore, the gut microbiome of animals fed a high-fat or high-sugar diet is more prone to circadian rhythm disruption . Studies also suggest that overwhelming systemic stress and inflammation—such as that induced via severe burn injury—can also produce characteristic acute changes in the gut microbiota within just one day of the sustained insult .
The microbiome in disease
Studies examining the composition and role of the intestinal microbiome in different disease states have uncovered associations with inflammatory bowel diseases (IBD), inflammatory skin diseases such as psoriasis and atopic dermatitis, autoimmune arthritis, type 2 diabetes, obesity, and atherosclerosis. For instance, IBD patients tend to have less bacterial diversity as well as lower numbers of Bacteroides and Firmicutes—which together may contribute to reduced concentrations of microbial-derived butyrate. Butyrate and other SCFAs are thought to have a direct anti-inflammatory effect in the gut . Furthermore, different indices of Crohn’s disease activity have each been characterized by specific gut mucosa-attached bacteria, that in turn are significantly influenced by anti-TNF therapy . The relative abundance of different bacteria may mediate intestinal inflammation and Crohn’s disease activity through effects on local regulatory T cell populations [17, 18]. Furthermore, overrepresentation analysis has shown that enzymes enriched in IBD microbiomes are more frequently involved in membrane transport, which could support a “leaky gut hypothesis” contributing to the disease state [19, 20]. Interestingly, autoimmune Th17 differentiation from naïve T cells appears to be dependent on the segmented filamentous bacteria. Studies have shown that Th17 cells are absent in the small-intestinal lamina propria of germ-free animals, which is the major site of their differentiation. Furthermore, introduction of segmented filamentous bacteria is sufficient to trigger autoimmune arthritis in these animals through promotion of Th17 cell development in the lamina propria and spleen [20, 21]. The gut microbiota of patients with type 2 diabetes has been functionally characterized with diabetes-associated markers, showing enriched membrane transport of sugars and branched-chain amino acids, xenobiotic metabolism, and sulphate reduction along with decreased bacterial chemotaxis, butyrate synthesis and metabolism of cofactors and vitamins . Obesity has been characterized by an altered intestinal Bacteroides:Firmicutes ratio, with greater relative abundance of Firmicutes. Furthermore, studies involving microbiota transplantation from obese to lean mice have shown that the obese phenotype is transmissible and may be promoted by microbiota that have increased capacity to harvest energy from the host diet . Risk of atherosclerosis has similarly been linked to the gut microbiota, in particular due to enhanced metabolism of choline and phosphatidylcholine that produces the proatherogenic compound, trimethylamine-N-oxide (TMAO) . A recent study also demonstrated that gut bacteria can produce significant amounts of amyloid and lipopolysaccharides, which are key players in the pathogenesis of Alzheimer’s disease . These observations illustrate the important role of microorganisms in human health and suggest that manipulating them may influence disease activity. While the microbiome of a healthy individual is relatively stable, gut microbial dynamics can certainly be influenced by host lifestyle and dietary choices .
Overview of select gut bacterial genera and species commonly affected by diet
Associated physiologic changes
Associated disease states
Gram positive obligate anaerobe branched; nonmotile
SCFA production; improve gut mucosal barrier; lower intestinal LPS levels
Reduced abundance in obesity
Gram positive facultative anaerobe rod-shaped
SCFA production; anti-inflammatory and anti-cancer activities
Gram negative obligate anaerobe rod-shaped; variable motility
Activate CD4 + T cells
Increased abundance in IBD
Gram negative obligate anaerobe rod-shaped; bile-resistant and pigment-producinga
Reported in tissue from acute appendicitis and perirectal and brain abscesses
Gram negative obligate anaerobe urease-positive, bile resistant, catalase-positive
Promote pro-inflammatory TH1 immunity
B. wadsworthia observed in colitis, perforated and gangrenous appendicitis, liver and soft tissue abscesses, cholecystitis, FG, empyema, osteomyelitis, and HS
Gram positive obligate anaerobe rod-shaped; spore-forming
Promote generation of TH17 cells
Several spp. are pathogenic causing tetanus, botulism, gas gangrene, or pseudomembranous colitis
Gram variable obligate anaerobe curved rod-shaped; motile
Reduced abundance in IBD
Gram positive obligate anaerobe rod-shaped
SCFA production; form beneficial phenolic acids
Reduced abundance in IBD
Gram positive facultative anaerobe cocci
Several spp. are pathogenic causing UTI, endocarditis, or bacteremia
Gram positive obligate anaerobe rod-shaped; nonmotile
SCFA production; anti-inflammatory effects
Reduced abundance in IBD and obesity
Gram negative obligate anaerobe oval-shaped; nonmotile
Reduced abundance in IBD, obesity, and psoriatic arthritis
Gram negative facultative anaerobe rod-shaped
Increased abundance in IBD gastroenteritis, UTI, and meningitis
Gram negative microaerophilic helix-shaped; motile
Gastritis; ulcers; MALT cancers
Gram positive facultative anaerobe cocci
Some spp. are pathogenic causing meningitis, pneumonia, and endocarditis
We performed a systematic literature review in September 2015 by searching the electronic MEDLINE database via PubMed. Search terms included combinations of the terms “microbiota”, “intestinal mucosa/microbiology”, “gastrointestinal tract/microbiology”, “gastrointestinal diseases/microbiology”, with “diet”, “food”, “polysaccharides”, “carbohydrates”, “proteins”, “meat”, “fat”, “lactose”, “oligofructose”, “prebiotics”, “probiotics”, “polyphenols”, “starch”, “soy”, “sucrose”, “fructose”, “diet, vegetarian”, “diet, western”, “cereals”, “dietary fiber”, and “dietary supplements”. Articles were reviewed independently by two investigators, R.K.S. and K.M.L, and this was adjudicated by W.L. We limited our search to articles available in English, human studies, and those published between 1970 and 2015. We excluded studies that did not explicitly address the effect of a dietary intervention on microbial composition. Manual searches through reference lists of the articles were also performed to identify additional studies. This resulted in a total of 188 articles being selected for inclusion in this review. Studies describing the relationship between specific dietary components and intestinal microbiota composition ranged from subject number n = 3 to n = 344, with a majority of studies clustered around subject number n = 20 to 70. Study designs were primarily randomized controlled trials, cross-sectional studies, case–control studies, and in vitro studies. In addition to human studies, several animal studies were also included to demonstrate dietary impact on the microbiome under controlled experimental conditions.
Diet and microbiota
Mouse studies have revealed that high protein intake increases insulin-like growth factor 1 (IGF-1) levels, which are in turn associated with an increased risk of cancer, diabetes, and overall mortality. In one study, plant-derived proteins are associated with lower mortality than animal-derived proteins . Accordingly, long-term practice of such dietary habits may increase risk of colonic disease and others. It is important to note that animal-based diets are often high in fat, in addition to protein. Dietary fat can also affect microbial composition; therefore, further studies will be required to investigate in what capacity each individual macromolecule impacts the bacterial communities and how they act in concert.
Digestible carbohydrates (starch, sugars)
The artificial sweeteners saccharin, sucralose, and aspartame represent another dietary controversy. Artificial sweeteners were originally marketed as a health-conscious, no-calorie food option that could be used to replace natural sugar. Recent evidence from Suez et al. suggests that consumption of all types of artificial sweeteners is actually more likely to induce glucose intolerance than consumption of pure glucose and sucrose. Interestingly, artificial sweeteners are thought to mediate this effect through alteration of gut microbiota. For instance, saccharin-fed mice were noted to have intestinal dysbiosis with increased relative abundance of Bacteroides and reduced Lactobacillus reuteri . These microbial shifts directly oppose those induced by intake of natural sugars (glucose, fructose, and sucrose)-as mentioned above. The evidence seems to suggest that, contrary to popular belief, artificial sweeteners may actually be unhealthier to consume than natural sugars.
Non-digestible carbohydrates (fiber)
In addition to their effects on the makeup of the microbiota, and likely partially mediated by these effects, prebiotics also produce notable shifts in metabolic and immune markers. For instance, several groups observed reductions in the proinflammatory cytokine IL-6, insulin resistance, and peak post-prandial glucose associated with intake of non-digestible carbohydrates present in whole grains [67, 78, 79]. One group additionally observed reductions in total body weight and concentrations of serum triglycerides, total cholesterol, LDL-cholesterol, and hemoglobin A1c . West et al.  noted increased plasma levels of the anti-inflammatory cytokine IL-10 with consumption of butyrylated high amylose maize starch. The beneficial effect of prebiotics on immune and metabolic function in the gut is thought to involve increased production of SCFAs and strengthening of gastrointestinal-associated lymphoid tissue (GALT) from fiber fermentation .
Other reported health benefits from consuming fermented dairy products include alleviation of GI intolerance symptoms [86, 100–102], accelerated intestinal transit time , increase in total serum IgA to potentiate the humoral immune response [90, 93, 94, 103], inhibition of pathogen adhesion to intestinal mucosa , and decreased abdominal distention and ascites in chronic liver disease patients . One study that analyzed stool from diarrhea-predominant IBS patients identified reduced abundance of Lactobacillus . Interestingly, Lactobacilli and Bifidobacteria have actually been used successfully for the prophylactic prevention of traveller’s diarrhea .
Effects of special diets on gut microbiota
High animal fat/protein
High fiber/antioxidants/UFA low red meat
Sanz et al. had 10 healthy subjects consume a gluten-free diet for 30 days. Populations of “healthy bacteria” decreased (Bifidobacterium and Lactobacillus), while populations of potentially unhealthy bacteria increased in parallel to reductions in polysaccharide intake after beginning the diet. In particular, increases were detected in numbers of E. coli and total Enterobacteriaceae, which may include further opportunistic pathogens . Bonder et al.  similarly investigated the influence of a short-term gluten-free diet, noting reductions in Ruminococcus bromii and Roseburia faecis with increased Victivallaceae and Clostridiaceae.
Vegan and vegetarian diets are enriched in fermentable plant-based foods. One study compared vegan and vegetarian diets to an unrestricted control diet, and found that both vegans and vegetarians had significantly lower counts of Bifidobacterium and Bacteroides species  (p < 0.001). Interestingly, another study found a very modest difference in the gut microbomes of vegan versus omnivorous subjects . The discrepancy between the two studies may be due to different methodologies for microbiome profiling (culture- vs sequencing-based), different control group diets, and/or host genetics. Future studies with careful experimental design will be needed to provide more insight into the differential effects of vegan and vegetarian diets on the gut microbiome.
Across the spectrum, the Mediterranean diet is highly regarded as a healthy balanced diet. It is distinguished by a beneficial fatty acid profile that is rich in both monounsaturated and polyunsaturated fatty acids, high levels of polyphenols and other antioxidants, high intake of fiber and other low glycemic carbohydrates, and relatively greater vegetable than animal protein intake. Specifically, olive oil, assorted fruits, vegetables, cereals, legumes, and nuts; moderate consumption of fish, poultry, and red wine; and a lower intake of dairy products, red meat, processed meat and sweets characterize the traditional Mediterranean diet . De Filippis et al. investigated the potential benefits of the Mediterranean diet by comparing habitual omnivores, vegetarians, and vegans. They observed that the majority of vegans and vegetarians, but only 30% of omnivores, had high adherence to the Mediterranean diet. They detected significant associations between degree of adherence to the Mediterranean diet and increased levels of fecal SCFAs, Prevotella bacteria, and other Firmicutes. At the same time low adherence to the Mediterranean diet was associated with elevated urinary trimethylamine oxide, which is associated with increased cardiovascular risk . Several other studies have shown that foods comprising the typical Mediterranean diet also improve obesity, the lipid profile, and inflammation. These changes may be mediated by diet-derived increases in Lactobacillus, Bifidobacterium, and Prevotella, and decreases in Clostridium [49, 110, 114, 130–132].
The ability to rapidly identify and quantify gut bacterial genera has helped us understand the impact of diet on host microbial composition. Studies that involve intake of a specific dietary component demonstrate how certain bacteria tend to respond to the nutrient-specific challenge. Protein, fats, digestible and non-digestible carbohydrates, probiotics, and polyphenols all induce shifts in the microbiome with secondary effects on host immunologic and metabolic markers. For instance, animal protein intake positively correlates with overall microbial diversity, increases abundance of bile-tolerant organisms such as Bacteroides, Alistipes, and Bilophila, and reduces representation of the Roseburia/E. rectale group. A high-saturated fat diet seems to increase counts of total anaerobic microflora and the relative abundance of Bacteroides and Bilophila. Human studies have not reported that a high-unsaturated fat diet significantly alters the gut bacterial profile; however, mouse studies have reported increases in Actinobacteria (Bifidobacterium and Adlercreutzia), lactic acid bacteria (Lactobacillus and Streptococcus), and Verrucomicrobia (Akkermansia muciniphila). Both digestible and non-digestible carbohydrates are commonly reported in the literature to enrich Bifidobacterium and suppress Clostridia, while only non-digestible carbohydrates are noted to additionally enrich for Lactobacillus, Ruminococcus, Eubacterium rectale, and Roseburia. Lastly, both probiotics and polyphenols enhance Bifidobacterium and lactic acid bacteria, while reducing enteropathogenic Clostridia species.
Maintaining a healthy gut microbiome is critical to human health
Effects of dietary components on immune parameters
Effects of dietary components on metabolic parameters
Conclusion and future directions
In conclusion, review of the literature suggests that diet can modify the intestinal microbiome, which in turn has a profound impact on overall health. This impact can be beneficial or detrimental, depending on the relative identity and abundance of constituent bacterial populations. For example, it has been shown that a high-fat diet adversely reduces A. muciniphila and Lactobacillus, which are both associated with healthy metabolic states . This observation provides a good example of how dietary intervention might potentially be used to manage complex diseases, such as obesity and diabetes. Furthermore, advances in microbiome research have suggested novel therapeutic possibilities for diseases that have traditionally been difficult to treat. For example, the fecal microbiota transplant has been used successfully to manage several different conditions, including ulcerative colitis, Clostridium difficile-associated colitis, irritable bowel syndrome, and even obesity [156–160]. It is possible that dermatologic conditions, including psoriasis and atopic dermatitis, may also be observed to benefit from re-engineering the gut microbiota. Recent advances in microbiome research offer exciting new tools to possibly enhance human health. Most of the studies reviewed in this manuscript profiled the microbiome using 16S rRNA amplicon sequencing, which utilizes the hypervariable regions of the bacterial 16S rRNA gene to identify bacteria present in biological samples. 16S rRNA sequencing is the most commonly used method by medical researchers to study microbial composition, due to its low cost and relatively easy workflow for sample preparation and bioinformatic analyses. However, 16S rRNA amplicon sequencing primarily provides information about microbial identity and not function. In order to investigate the microbiome’s functions, many researchers have turned to a shotgun metagenomic approach in which the whole bacterial genome is sequenced. Despite a higher cost and more complicated bioinformatics requirement, shotgun metagenomics provides information about both microbial identity and gene composition. Knowing which genes are encoded by the bacteria present in a sample allows researchers to better understand their roles in human health. With reducing costs of next generation sequencing, improved sample preparation protocols, and more bioinformatic tools available for metagenomic analysis, this technique will be a powerful tool to study microbiome functionality. Performing meta-analyses to correlate the microbiome with host genomes, transcriptomes, and immunophenotypes represents another exciting avenue for investigating human and bacterial interactions.
Precision medicine is another attractive, novel therapeutic approach for many diseases with strong genetic associations. It is important to note that the host genotype also plays a role in shaping the microbiome, and that this host-microbe interaction is crucial for maintaining human health . Therefore, a better understanding of the interplay between genes, phenotypes, and the microbiome will provide important insights into the utility of precision medicine.
The observation that diet can modulate host-microbe interactions heralds a promising future therapeutic approach. Already, the gut microbiome has been found to influence the response to cancer immunotherapy [162, 163]. Indeed, personalized nutrition is an emerging concept that utilizes a machine-learning algorithm to predict metabolic responses to meals [164, 165]. This tool has broad implications for individualized patient care through dietary modification. While this and other technology is in the process of being refined and validated, further research using large, long-term clinical trials to evaluate a greater variety of food components would be helpful in making specific dietary recommendations to patients.
gut-associated lymphoid tissue
high-sensitivity C-reactive protein
inflammatory bowel disease
irritable bowel syndrome
insulin-like growth factor-1
microbiota accessible carbohydrate
very low-density lipoprotein
WL and TB conceived and supervised the work. RKS, HC, DY, KL, DU, KW, MA, BF, MN, and TZ performed data acquisition. RKS, HC, and DY performed data analysis and wrote the manuscript. All named authors meet the International Committee of Medical Journal Editors (ICMJE) criteria for authorship for this manuscript, take responsibility for the integrity of the work as a whole, and have given final approval for the version to be published. All authors read and approved the final manuscript.
We are grateful to the Dinsmore family for their support of this project.
Dr. Wilson Liao serves as a research investigator for Abbvie, Janssen, Pfizer, and Novartis. Dr. Tina Bhutani is an advisor for Cutanea and conducts research for Abbvie, Janssen, and Merck. Dr. Liao and Dr. Bhutani have no stocks, employment or board memberships with any pharmaceutical company. The remaining authors have nothing to disclose.
Availability of data and materials
The data supporting the conclusions of this article are included within the article.
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This article does not contain any individual person’s data in any form.
Ethics approval and consent to participate
This article does not involve any new studies of human or animal subjects performed by any of the authors.
Dr. Wilson Liao is supported in part by grants from the National Institutes of Health (R01AR065174, U01AI119125).
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