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The Impact of Diet and Lifestyle on Gut Microbiota and Human Health

Abstract: There is growing recognition of the role of diet and other environmental factors in modulating the composition and metabolic activity of the human gut microbiota, which in turn can impact health. This narrative review explores the relevant contemporary scientific literature to provide a general perspective of this broad area. Molecular technologies have greatly advanced our understanding of the complexity and diversity of the gut microbial communities within and between individuals. Diet, particularly macronutrients, has a major role in shaping the composition and activity of these complex populations. Despite the body of knowledge that exists on the effects of carbohydrates there are still many unanswered questions. The impacts of dietary fats and protein on the gut microbiota are less well defined. Both short- and long-term dietary change can influence the microbial profiles, and infant nutrition may have life-long consequences through microbial modulation of the immune system. The impact of environmental factors, including aspects of lifestyle, on the microbiota is particularly poorly understood but some of these factors are described. We also discuss the use and potential benefits of prebiotics and probiotics to modify microbial populations. A description of some areas that should be addressed in future research is also presented.

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Alex’s Notes: Some of the most well-known gut bacteria genera in adults are Bifidobacterium, Lactobacillus, Bacteroides, Clostridium, Escherichia, Streptococcus, and Ruminococcus. Although we may have several hundred species of microbes within our guts, findings from The Human Microbiome Project have shown that thousands of species of microbes may inhabit the guts of humans collectively, and that there is a huge amount of variation between persons. There is also an increasing focus on associations between gut microbes and disease, which is not surprising given the numerous bioactive compounds that these little guys produce.

The bioactive products produced ultimately depend on numerous factors, and most will be taken up by gastrointestinal (GI) tissues, potentially reaching circulation and other bodily tissues. The most abundant and physiologically important end-products are short-chained fatty acids (SCFAs) that act as a central energy source for colon cells, and may even reach circulation to impact immune function and inflammation in tissues such as the lungs. SCFAs are produced through the fermentation of fibers, which are non-digestible carbohydrates. Conversely, fermentation of some proteins produces potentially toxic compounds such as ammonia, phenols, and hydrogen sulphide.

Whatever the substrate, it is clear that many enzymes produced by microbes influence digestion and health and that many microbes are needed for a somewhat step-wise breakdown and use of compounds that escape our own enzymatic digestion. For instance, bacterial phytases of the large intestine degrade the unfairly vilified phytic acid present in grains, which releasing the minerals such as calcium, magnesium, and phosphate that are bound to it, making them available for absorption. Similarly, many bacteria metabolize our intestinal mucosal layers to meet their energy need, which assists in our natural and rapid turnover of this critical barrier.

There is also competition between microbes. Hydrogen is a currency that creates an economy based around production by some organisms and usage by others. Microbes which produce methane (Archaea) exist in about 50% of individuals and compete with SCFA-producing bacteria for this valuable element. This not only has potential health consequences through limiting the production of beneficial SCFAs, but also potential social impacts as methane is the main ingredient in “silent but deadly” gas bombs. Similarly, some bacteria such as Faecalibacterium prausnitzii may produce anti-inflammatory compounds.

And it all starts at birth

The fact that vaginal birth results in greater microbial counts within infant guts compared to caesarean section suggests that gut colonization begins with the birth process. This continues through breastfeeding where the oligosaccharides present in breast milk promote the growth of Lactobacillus and Bifidobacterium, and there is a major shift in bacterial populations with the switch to solid foods and a more varied diet. Functional maturation of the microbiome continues to increase with age.

As we mature, our lifestyle habits play a significant role on our guts. For instance, smoking and a lack of exercise are major risk factors for colorectal cancer, suggesting they may interact with the microbiome. Sure enough, smoking has been shown to influence the gut microbe composition in healthy persons, leading to increased levels of Bacteroides-Prevotella. Similarly, there may be a link between air pollution in general and intestinal diseases. As for exercise, a very recent study found significantly greater microbe diversity in professional athletes, and both human and animal models of obesity show increases in Firmicutes and reductions in the Bacteroidetes, which could potentially contribute to increased adiposity through greater energy harvests. However, other data suggests that the shifts in microbial communities seen with obesity are primarily driven by high-fat obesogenic diets. It has been suggested that dietary saturated fats may increase the number of pro-inflammatory microbes through the formation of taurine-conjugated bile acids.

Another overlooked lifestyle factor – stress – may also impact microbiome profiles through the gut-brain axis. Stress is associated with lower numbers of the potentially beneficial Lactobacillus bacteria, and since the axis is bidirectional, changes in the microbiome may in turn influence brain activity, including mood.

Even geography plays a role as we age, if for no other reason than that of the dietary and environmental exposures it standardizes for us. Children from rural Africa have shown greater microbe diversity compared to more developed communities, including more fiber-metabolizing strains, and the types of bacteria common to persons from the USA significantly differ from persons living in rural areas of Venezuela and Malawi.

Speaking of diet

An adult colon receives numerous amounts of different compounds on a daily basis. This includes fibers, proteins, lipids, sugar alcohols, and various other minor dietary constituents such as polyphenols, catechins, lignin, tannins, and vitamins and minerals.

Carbohydrates are by far the most important energy source for the microbiome, so is it any wonder that fiber is consistently shown to benefit health? Even non-fermentable fibers such as cellulose play a role through absorbing water and increasing fecal mass, thereby diluting toxins, reducing intracolonic pressure, and shortening transit time to increase defecation frequency. Nonetheless, most fiber health benefits come from fermentation of carbohydrates into SCFAs that provide energy for other microbes and colon cells while inhibiting the growth and activity of pathogenic bacteria. Acetate, propionate, and butyrate are the major individual SCFAs, accounting for 90% of the total, with ratios of about 65:20:15.

Dietary protein also has a significant impact on the gut, which can be beneficial or harmful depending on the context of protein consumption. Many previous epidemiological studies have found an association between colorectal cancer and consumption of red meat, although more recent evidence suggests that it is processed meats rather than the meat itself that garners the risk. Regardless, dietary protein serves as the principal source of nitrogen for microbial growth and the assimilation of beneficial products. Fermentation of proteins produces a much greater diversity of by-products including ammonia, hydrogen sulphide, amines, phenols, thiols, and indoles, all of which have been shown to be cytotoxic, genotoxic, and carcinogenic. That said, higher protein intakes do not always result in higher levels of these products, nor does it increase the genotoxicity in humans.

Dietary fat is much less studied with regard to its impact on the gut. High-fat diets in humans increase circulating levels of pro-inflammatory lipopolysaccharides (LPS), possibly through increased gut permeability. The impact of dietary fat may also be mediated indirectly through bile acids, which are necessary for fat digestion and absorption. As fat intake increases, so does the number of bile acids entering the colon to be fermented by bacteria into potentially carcinogenic secondary bile acids.

Overall, it is important to keep in mind that much data about the microbiome comes from analysis of Caucasian adults habitually consuming a Western diet, which is associated with countless diseases and characterized by the over-consumption of highly refined, omnivorous foods of poor nutritional quality and low in fiber. Add in the habitual sedentary behavior and we have a recipe for disaster.

But change is possible

Replacing a habitual Western diet with on high in fiber elicited rapid (within 24 hours) changes in microbiome composition. Similarly, altering dietary energy load in lean and obese adults causes changes in the proportions of Bacteroidetes and Firmicutes, with the former decreasing while the latter increases with increasing energy intake. High-fat diets have shown to alter the gut composition independently of obesity, resulting in fewer numbers of Bacteroidetes and increased numbers of Firmicutes and Proteobacteria. High-fat diets also reduce Bifidobacterium numbers and increase circulating LPS concentrations, promoting endotoxemia and systemic low-grade inflammation.

We yet must not forget about n=1, however. For instance, some individuals have low levels of butyrate despite increasing levels of fibrous substrate. There are also strong inter-individual differences in our ability to metabolize certain compounds.

These are the gate-keepers, after all

Our entire GI tract is lined with mucus that acts as a barrier to microbial invasion. Although some bacterial end-products like SCFAs can stimulate the production of muscus and mucus breakdown by bacteria is a normal part of mucus turnover, over-utilization of the mucus by bacteria such as Akkermansia muciniphila can lead to a thinning of the barrier and possibly tissue inflammation. This loss of integrity is better known as “leaky gut.” A significant portion of immune system activities occur within the gut, and it has been suggested that distress which leads to increased permeability and subsequent immune changes early in life may have vast implications down the road.

An interesting example of the above is Parkinson’s disease. Persons with this multi-system dysfunction have increased intestinal permeability, greater LPS exposure, and increased mucosal barrier breakdown. These changes in the gut correlate with the degree of neuronal damage, suggesting that pathogens may play a role in the etiology of Parkinson’s disease. An impaired gut barrier may also play a role in insulin resistance, obesity, type-2 diabetes, cardiovascular disease, metabolic syndrome, and even autism.

Is there a place for supplementation?

This is a valid question. If a healthy microbiome is so central to health, then it only makes sense to supplement with probiotics and prebiotics in order to promote colonization of beneficial microbes.

Prebiotics are dietary compounds that selectively promote the growth of “beneficial” bacteria, and soluble fibers are the hallmark substance. The most well-known fibers prebiotics include inulin-type fructans, fructo-oligosaccharides, galacto-oligosaccharides, beta-glucans, pectins, and resistant starches. Animal models provide strong evidence of the potential of prebiotics to protect against a range of chronic diseases. However, the inter-individual variability in the microbial response to resistant starch suggests that successful prebiotic interventions would need to be personalized.

Probiotics are basically what prebiotics aim to nourish within the gut, except that they are packaged inside a pill for consumption. The basic idea is that by consuming probiotics, the bacteria within the pill will colonize the colon with “beneficial” bacteria. Of course human studies on this are equivocal, with differences in results likely being caused by differences in methodologies and sample populations. Additionally, it is clear from in vivo studies that the health promoting effects are strain dependent, not species or genus specific, and that any changes in the microbiome are small in magnitude and only persist for the duration of supplementation. Finally, while probiotic supplementation has practical relevance for promoting health, the concept is simplistic given our current limited understanding of the complex and dynamic nature of the microbiome and its host-interactions.

So how can we understand?

First and foremost, there is a growing need for an understanding of the activities of gut microbes, especially with regard to their host-physiology relevance. What role specifically do different microbes play in the breakdown of food and its associated by-products? Similarly, understanding which foods strengthen or weaken the mucus barrier of the gut may help in tailoring diets so as to prevent leaky gut and endotoxemia. Since the gut-brain axis is bidirectional, understanding which microbes have effects that reach the CNS may allow for treatments of mental health conditions as well as a better understanding of how dietary manipulations impacts cognition. Perhaps many of these goals and more could be accomplished with studies that follow the development of microbial populations through life in persons around the world. It would not be the first time studies spanning decades would have been conducted. For instance, the Genetic Studies of Genius cohort of 1,528 persons from the U.S. has been ongoing since 1921.

We must also further our understanding of the food we consume and its interactions with our microbiomes. Ian Spreadbury recently proposed that dense acellular carbohydrates promote an inflammatory microbiome. These are the carbohydrates found in flours and refined grains, as opposed to water-diluted cellular carbohydrates of fruits, vegetables, and tubers.

 
 

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