Essential Factors for a Healthy Microbiome: History
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Contributor:
Patricia Grace-Farfaglia
,
Heather Frazier
,
Maura Daly Iversen

Recent discoveries of the purpose and potential of microbial interactions with humans have broad implications for our understanding of metabolism, immunity, the host–microbe genetic interactions. Bioavailability and bioaccessibility of phytonutrients in foods not only enrich microbial diversity in the lower human gastrointestinal tract (GIT) but also direct the functioning of the metagenome of the microbiota. Thus, healthy choices must include foods that contain nutrients that satisfy both the needs of humans and their microbes. Physical activity interventions at a moderate level of intensity have shown positive effects on metabolism and the microbiome, while intense training (>70% VO2max) reduces diversity in the short term. The microbiome of elite endurance athletes is a robust producer of short-chain fatty acids. A lifestyle lacking activity is associated with the development of chronic disease, and experimental conditions simulating weightlessness in humans demonstrate loss of muscle mass occurring in conjunction with a decline in gut short-chain fatty acid (SCFA) production and the microbes that produce them.

  • microbiome
  • diet
  • lifestyle
  • physical activity
  • microbial diversity
  • microbial density

1. Introduction

Microbial species in the gut, including fungi, viruses, and bacteria, are key influencers in human development, immune function, and health. The gut microbiome functions as both a nutritional competitor and supplier of nutraceuticals and facilitates human metabolism. In this way, the microbiome behaves as an economy that trades in nutrients and the end products of fermentation; thus, supply and demand forces may apply. Economists have observed that developing countries often suffer from the paradox of plenty, such that resource riches lead to marginalization and poverty in some groups [1]. The “resource curse” framework can be applied to the human microbiome, where richness in some nutritional components leads to bacterial overgrowth of certain species, thus crowding out the growth and sustainability of others [2]. The western pattern diet (WPD) due to its nutrient resources which are low in fiber and carbohydrate polymers of 10 or more monomeric units, disrupts microbial populations resulting in damage to the intestinal epithelial barrier (IEB)–the gatekeeper of nutrient permeability into the endothelium [3]. Once the intercellular junction has been breached, inflammation and tissue injury occur. Pathogens take advantage of this disruption, while commensal bacteria become displaced by dysregulation. Resource imbalance creates a lack of “leadership” among microbes and results in a lawless state of dysbiosis where some species go into decline.
The formation of the protective mucous barrier on the lining of the intestinal lumen creates a physical space for the host–microbe exchange of nutrients and metabolites [4]. In addition, the production of short-chain fatty acids (SCFAs) through the fermentation of polysaccharides supports the energy needs of endothelial cells [5]. Commensal bacteria also play a key role in the post-natal development of the gut-associated immune system by regulating immune homeostasis, thus providing another defense mechanism against invading pathogens [6]. The adoption of dietary patterns must be viewed within a broader context of a system of interactions between the host and its microbiome.
Physical activity (PA) has been shown to prevent and treat a number of chronic diseases, including heart disease, type 2 diabetes, high blood pressure, some cancers, depression, and dementia [7]. In an experiment using dry immersion to simulate extreme inactivity while controlling for diet, researchers observed that participants not only developed muscle loss, but experienced a reduction in microbial production of propionate and an increase in Firmicutes [8]. Studies on habitual athletes have shown that they also have high levels of Firmicutes, but individual species vary by sport and activity level [9]. The gut microbiome of sedentary adults in a short-term exercise intervention given supplemental protein developed an increase in microbial and viral diversity [10]. However, one would expect that when athletes are compared to sedentary individuals that bacterial species associated with health would be more abundant in the more active group, as well as a greater consumption of fruits and vegetables [9].

2. Microbiome

The microbiome is a collection of bacteria, fungi, and viruses that varies by location, age, health status, diet, and physical activity levels. The dominant bacterial phyla in the human microbiome are  Firmicutes, Bacteroidetes, Proteobacteria, Actinobacteria, and Verrucomicrobia [11]. Most fungi are poor colonizers of the gastrointestinal tract (GIT), but seven taxa have been found: C. albicans, Saccharomyces cerevisiae, A. niger, Penicillium sp., Pichia, Aspergillus, and Mucor and are influenced by diet and alcohol consumption [12]. Candida is the most abundant genus in the first six weeks of life in infants, with colonization being greater in those delivered vaginally [13]. Bacteria reside in the gut, as well as other body sites (genital, skin, airway)—each with its own distinct population of archaea, viruses, and eukaryotes [14]. A healthy microbiome exhibits greater microbial diversity. Low microbial diversity is observed in disease states such as cardiovascular disease, cancer, obesity, and metabolic and immune disorders. The reduction in populations within the human microbial ecosystem or intestinal dysbiosis is associated with negative health effects [15].
The viruses (virobiota) and their communities (viromes) cross the IEB and are believed to have a cooperative evolution and symbiotic relationship with their host [16]. Viral colonization of the GI tract begins after birth and gradually increases with age [17]. Human endogenous retroviruses (HERVs) have entered host germ cells, eggs, and sperm, over successive generations of infecting our ancestors and make up approximately 8% of our genome [16]. HERVs can be coopted into protecting the host and participating in protective metabolic activities such as neuroprotection and embryonic development. Activation of HERVs can affect the expression of genes involved in immunity and inflammation. Researchers demonstrated that the fasting or overfed condition affected the expression of ERV-related genes in geese, suggesting that they are influential mediators in the development of non-alcoholic liver disease [18].

3. Diet

Individuals have unique gut microbial communities due to differences in host genetics, physical activity, aging, health, and dietary composition [19][20][21][22]. Food provides nutrients and other substrates for the bacteria that reside in the gut; in return, bacteria yields not only SCFAs, but significant amounts of vitamins K2 and B12, folate, riboflavin, thiamine, and other nutrients [23][24]. Interspecies bacterial competition for life-sustaining resources drives community composition [25]. To reduce dysbiosis and systemic inflammation, a better understanding of how strain diversity, their interactions, and the metabolism of various nutrients is crucial.
The habitual diet has wide-ranging effects on human health now and in the future. Telle-Hanson, Holven, and Ulven (2018) reviewed the literature on diet and its components, microbiota, and evidence of inflammation in dietary intervention trials to develop insight into the origin of cardiovascular disease [26]. Few conclusions were made due to the heterogeneity of factors and wide latitude in which the authors of the primary studies define a “healthy diet”. Data from the American Gut Project demonstrates that plant-based and flexitarian dietary patterns with higher Healthy Eating Index 2010 (HEI-2010) scores were associated with microbiome β-diversity or the extent of change in the number of microbial communities [27]. Diets rich in inflammatory foods such as refined grains, processed and red meats, fried foods, and added sugars are major factors in the causation of chronic diseases. Tools such as the Dietary Inflammatory Index (DII) are used to evaluate the inflammatory potential of an individual’s dietary pattern [28]. Fruits, vegetables, whole grains, and legumes consumption are all linked to the reduction of systemic inflammation as well as microbial diversity [29]. Consumption of whole fruits, vegetables, and legumes in a Mediterranean dietary pattern has been shown to increase fecal short-chain fatty acid (SCFA) levels, mainly due to fermentation of insoluble fibers by the most abundant phyla—Firmicutes and Bacteroidetes [30][31]. Grape and red wine, with their high polyphenol content, have been associated with beneficial changes in GIT microbial composition Proteobacteria, Fusobacteria, Firmicutes, Bacteroidetes, and B. uniformis [32]. The response to the consumption of 100% fruit juice varies by type, but orange juice has a positive effect on the gut microbiome [33][34]. The data from a short-term human trial using cherry juice suggests that participants who consumed a Western-style diet showed different gut microbiota responses than other participants due to their reduced ability to metabolize polyphenols [35]. Healthy volunteers in a month-long trial of Montmorency tart cherry concentrate had no change in species richness or microbial composition [36]. Thus, habitual dietary pattern affects the ability of individuals to receive all of the health benefits from fruits and vegetables.
In a study of food frequency and related bacterial genera in 98 participants, the authors reported that the habitual diet was correlated with separate clusters, termed “enterotypes,” primarily dominated by Bacteroides, Prevotella, and Ruminococcus [37]. The resulting dietary-enterotype framework showed that Bacteroides entero-type was highly associated with a more Westernized diet high in animal protein and saturated fats, while the Prevotella enterotype was associated with a carbohydrate-dominated diet. Vegetarians showed a mixed pattern of Prevotella and Bacteroides. Investigators in this controlled feeding trial demonstrated that by changing the diet pattern on a short-term basis to either a plant-based or animal-based diet, microbial community structure recovered to baseline bacterial composition once participants resumed their usual diet [38].
Nutrient-dense foods are higher in nutrients and lower in calories and naturally contain vitamins, minerals, fiber, or resistant starches. The MAL-ED study (Etiology, Risk Factors, and Interactions of Enteric Infections and Malnutrition and the Consequences for Child Health) followed a cohort of 1283 children ages 9 to 15 months from eight low resource populations to determine their risk of anemia, low retinol, zinc, ferritin, and high transferrin receptor (TfR) [39]. The researchers assessed diet intake, nutrient density, micronutrient status, and markers of inflammation. The authors concluded that after accounting for dietary nutrient density, there was an independent association between biomarkers of intestinal permeability and micronutrient status for children with anemia, low ferritin, and retinol levels. These data suggest that a nutrient-dense diet may be useful in reducing systemic inflammation.
A trial of a Mediterranean diet with an additional green tea supplement and minimal amounts of meat demonstrated improvement in cardiometabolic risk, weight loss, and changes in microbial abundance driven by a small low abundant non-core change in taxonomic composition [40]. The addition of a polyphenol-rich green tea supplement to the diet enhanced the abundance of Prevotella and Bifidobacterium involved in the synthesis and degradation of branched-chain amino acids. The presence of the genera Prevotella and Bifidobacterium is common in non-Western societies, and some authors have suggested that it may be a biomarker for a healthy lifestyle [41].

3.1. Western Diet

The Western-style diet, an energy-dense and nutrient-poor pattern, consists of processed meats, full-fat dairy such as cheese and ice cream, refined grains, and added sugars, which promote inflammation and chronic disease. A systematic review of 46 studies that measured the effect of Western food choices on inflammation concluded that “balanced” diets reduce the risk for chronic disease [42]. Across the 46 studies meeting inclusion criteria, individuals consuming Western-type and meat-based diets had higher markers of low-grade chronic inflammation. Results from studies on the MedDiet, a diet rich in fruits and vegetables, demonstrate that individuals following this type of diet have lower markers of low-grade inflammation. As these studies were drawn from cross-sectional observational designs, the authors concluded that in order to confirm these results, prospective trials are needed.

3.1.1. Ultra-Processed Foods

One discriminating feature between traditional and Western dietary patterns is the consumption of ultra-processed foods. The Open Food Facts database, which gathers food product information from around the world, uses the NOVA classification system to score products [43]. This system of classification has been used in cross-sectional studies of diet intake and chronic disease [44]. The NOVA classification of food has four categories: unprocessed or minimally processed foods, processed culinary ingredients, processed foods, and ultra-processed food and drink products. A systematic review and meta-analysis of cross-sectional studies on the effect of exposure to ultra-processed foods (UPF) on health status using food frequency and 24 h recall data found an increased risk of overweight, hypertension, metabolic syndrome, and low high-density lipoprotein [45]. The authors also reviewed five quality prospective-cohort studies and found an increased risk of all-cause mortality (RR 1.25, 95% CI 1.14, 1.37; p < 0.00001) for individuals who consumed elevated levels of UPF.
Food processing adds sodium, sugar, and other additives to modify the flavor, texture, and/or color. The influence of high sodium diets (HSD) is attributed to aberrant T-cell activation resulting in essential hypertension and other autoimmune diseases [46]. Experimental evidence using a rat model suggests that dietary sodium also alters the composition of gut microbial taxa, specifically Christensenellaceae and families, as well as the Erwinia and the Anaerostipes genera [47]. HSD also elevated levels of proteinuria and produced hypertension, a finding in agreement with human studies [48]. A randomized, double-blind, placebo-controlled crossover trial of a reduced-sodium diet in 145 untreated hypertensive individuals ages 30 to 75 years demonstrated increased circulating levels of SCFAs and decreased blood pressure [49]. Results for women showed a significant difference in all eight SCFAs, but there was no difference by race. In another study, a high sodium diet consumed by healthy volunteers was associated with an increase in blood pressure and an increased abundance of Prevotella, Bacteroides, and Ruminococcaceae [50]. Since “enterotypes” associated with diet have been described as being either Prevotella or Bacteroides dominant, this may suggest that there is a transition point from healthy to unhealthy, making this shift a marker for wellness [41].
Components of a processed diet may include the use of additives, particularly titanium dioxide (TiO2) and emulsifiers. These components influence the integrity of the IEB, while food additives promote biofilm formation, altering microbial composition [51][52][53][54][55][56]. Another role of food processing is the enrichment of foods with vitamins, minerals, and nutraceuticals according to regulations or for product marketing. By increasing nutrient density, fortification promotes biofilm formation under these conditions and promotes bacterial persistence to antibiotics.
Consumption of ultra-processed foods may induce low-grade gut inflammation and increase an individual’s risk for cancer and cardiovascular disease. An online survey of consumers found that they readily identified ultra-processed foods as foods being ready-to-eat and containing additives, food colorings, preservatives, and stabilizers [57]. Low-income consumers choose foods that are ultra-processed for several reasons, such as cost, convenience, and taste [45][58]. Public health educators should focus on educating consumers about how to make smarter choices by reading the food label and choosing products with few additives and minimal processing.

3.1.2. Protein

The degradation of dietary protein occurs through human and microbial proteases. Bacteria rely on carbohydrates and fiber for energy, but they are flexible and will use protein as an energy source when carbohydrate resources are low. Proteolytic fermentation produces phenols, branch-chain amino acids, sulfides, indoles, and ammonia as by-products [59]. Unlike the products of carbohydrate fermentation, colonic protein metabolites are often associated with colon cancer [60]. Researchers in one controlled human trial found that a three-week high protein diet had the effect of regulating the production of bacterial metabolites, causing an increase in the degradation of amino acids in the gut and modifying gut mucosal genes involved in cell cycle regulation [61]. Using a Human Intestinal Microbial Ecosystem (SHIME(R)) model researchers demonstrated that a high-protein diet (2.5 g/L casein) produces a different microbial community composition than a high-fiber (0.6 g/L casein) diet [62]. High-protein diets fed to mice lead to the development of obesity which was a major factor in shifting the gut microbial populations, but this effect was dependent on the diet’s protein-to-sucrose ratio [63].
One outcome of consuming diets rich in the essential amino acid tryptophan, such as dairy, poultry, and nuts, is that they favor the generation of indole and indole derivatives by colonic bacteria. Indole is a signaling molecule that regulates the host immune system by supporting epithelial barrier defense in a way that controls pathogens without producing an inflammatory response [64][65], thereby reducing chronic inflammation caused by the passage of bacteria and toxins from the gut into the bloodstream [66].

3.1.3. Fats

Trans-fat, or trans-fatty acids, are a by-product of the hydrogenation of vegetable oils to enhance shelf-life and other desirable food characteristics. Once considered to be a healthier alternative to saturated fat, there is now a consensus on the role trans fatty acids play in the development of heart disease and stroke by increasing LDL cholesterol and reducing HDL cholesterol. The association of high intakes of iTFA (industrial trans-fats) with cardiovascular disease has led to public health recommendations to reduce or eliminate their use. High intake of iTFA in mice has been shown to cause significant dysbiosis of gut microbiota [67]. A survey of the consumption of industrial trans-fatty acids reported that 22 out of 29 countries sampled found the intake of total trans-fat is currently below recommendations of 1% [68].
The ability of colonic bacteria to adapt to a fats-only source of energy for bacterial growth has been demonstrated in a fats-only medium through genes encoding for enzymes involved in fat degradation [69]. In the fats-only condition, Alistipes spp., Bilophila spp., and total Proteobacteria were favored, while SCFA-producing species, such as Bacteroides, Clostridium, and Eubacterium spp., declined. Through the use of an in vitro human gut simulator (HGS) model, the authors also demonstrated that in a fats-only medium fortified with micronutrients that lack protein or carbohydrate, bacterial communities responded with a change in community structure [69]. Colonic bacteria adaptation to a fats-only diet comes at a price to the host through a reduction in the absorption of antioxidants and an increase in the expression of bacterial virulence factors [70]. In a systematic review of the MyNewGut project data, researchers found that diets high in saturated fats degreased both richness and diversity, while those high in monounsaturated fatty acids (MUFA) produced a lower total number of bacteria, whereas a diet rich in polyunsaturated fatty acids (PUFA) resulted in no change [71].

3.1.4. Carbohydrates and Fiber

WPDs are comprised of highly refined sugars, particularly sucrose and fructose. It has been suggested that one of the causes of obesity may be an adaptation in microbial diversity due to one or more components in the Western diet [72]. Researchers using a mouse model reported that a diet high in fructose and/or sucrose, a pellet with 55% fructose-42% glucose ratio, alters the ratio of Bacteroidetes to Proteobacteria, favoring the profile associated with metabolic syndrome [73]. Metabolic syndrome increases an individual’s risk for cardiovascular disease and type 2 diabetes. Lifestyle intervention research using diet and physical activity approaches has only been partially successful in controlling the epidemic of obesity.
Diets high in fermentable carbohydrates and fiber alter the nutritional ecology of bacteria resulting in bacterial diversity, particular species that produce SCFAs such as butyrate, acetate, and propionate, as well as lactate and gasses (CO2, H2, and CH4) [59]. In a study of pregnant women, low fiber intake was associated with a gut microbiota profile favoring the fermentation of lactate and insulin resistance, while a diet rich in fruits and vegetables promoted bacteria that produce SCFAs through bacterial fermentation of plant polysaccharides [74]. Incorporating healthier eating behaviors into prenatal counseling may support a more beneficial gut microbiome.
Naturally sweet foods such as honey have long been known to have both antimicrobial and probiotic properties, although it is primarily glucose and fructose [75]. Honey promotes commensal strains such as Lactobacillus reuteri, Lactobacillus rhamnosus, and Bifidobacterium lactis while limiting the growth and adhesion of pathogenic bacteria in the host. North American maple syrup is rich in phytochemicals and oligosaccharides, as well as lignin [76][77]. Maple syrup improved insulin sensitivity and reduced non-alcoholic fatty liver in a diet-induced obese insulin-resistant rat model [78]. A randomized controlled trial in humans on the role of maple syrup on gut microbial diversity and metabolic syndrome in humans is currently underway [79].
Fermented foods are processed using techniques for “controlled microbial growth” to produce enzymes that alter food characteristics [80]. Food and beverage products have traditionally been either fermented, aged, or inoculated with bacteria and yeasts to preserve and enhance their flavor. Studies on the impact of fermented foods on the gut microbiome suggest they have a positive impact on the gut microbiome, but the quality of the evidence is unclear [81]. The generalizability of health benefits from fermentation is limited due to the undefined microbial content of starter cultures and the uniqueness of each processing plant’s bacteria and fungi communities [82]. The fermentation process has potential positive impacts, such as the release of bioactive peptides, biogenic amines, and phenolic compounds with increased antioxidant activity. Bioactive peptides and polyamines have beneficial effects on cardiovascular, immune and metabolic health, such as enhanced mineral absorption and reduced oxidative stress [83].
In addition to acting as the food source for intestinal bacteria-resistant starches, polyphenols and fiber have been shown experimentally to modulate the quantity and composition of microbiota by inducing prophages, virus-like-particles (VLPs) [84]. These bacteriophages protect the gut lining from pathogens and insert into the genome of their host’s chromosomal DNA as prophages. The bactericidal effects of VLPs are triggered by several common foods and products such as Tabasco sauce, vinegar, Kombucha, cinnamon, miso, oregano, coffee Arabica, and stevia. Although stevia appears to have positive effects on gut microbiota, it can induce heritable changes in gene expression in offspring. Experimental evidence of a recent study on the effect of maternal stevia consumption on obese rats fed a diet high in fat/sugar (HFS) combined with either aspartame or stevia resulted in second-generational effects of obesity and glucose intolerance in the offspring [85]. The proposed mechanism for the observed effect was the development of altered gene expression in the mesolimbic reward pathway associated with feeding behavior.
In the past, the mechanism behind the observed beneficial health effects of cultural superfoods, such as natto and kimchi, was unknown [86]. In the future, diets may be personalized to enhance the ecology of the gut microbiome through the targeted use of these foods.

3.1.5. Diet Supplementation

The quality of the diet shapes the health of the host and gut. For example, vitamin A deficiency has an effect on microbial community structure and gene expression [87]. The development of the gut microbiome in infancy and childhood is affected by the supply of micronutrients in the diet [88]. In regard to micronutrient supplementation, a study of Kenyan infants concluded that iron fortification adversely affects the gut microbiome by significantly increasing the population of pathogens, such as Clostridium and Escherichia/Shigella, with a reduction in beneficial Bifidobacterium which increases inflammation [89]. The authors of the study concluded that when iron is poorly absorbed by the small intestine, the resulting iron overload in the colon disrupts the bacterial population. The effect of iron and zinc fortified foods on gut microbiota was reviewed in one systematic review, and the authors reported no adverse effects in the five studies retrieved [90]. With the widespread fortification of food products to promote health and prevent nutrient deficiencies, more research on the effects of biofortification on gut bacterial populations is needed.

3.1.6. Water

Data from the American Gut project database suggests that drinking water source is associated with microbiota composition [91]. Fecal samples from individuals who consumed well water had greater β-diversity compared to those who drank bottled, filtered, or tap water. Dai et al. reported that microbes coming from drinking water supplies that have been disinfected versus non-disinfected water have a less diverse structure and function, favoring microbes that utilize fatty acids derived from microbial decomposition [92].

This entry is adapted from the peer-reviewed paper 10.3390/ijerph19148361

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