Gut microbiome changes induced by a diet rich in fruits and vegetables

Abstract

Habitual dietary intake is a major determinant of the species composition and functional output of the trillions of microorganisms residing in the human gut. Diet influences which microbes will colonise, flourish or disappear throughout life. An increase in polyphenols, oligosaccharides and fibre, which are all components found in a fruit and vegetable-rich diet, have long been associated with decreased risk of chronic diseases. Many of the benefits induced by this type of diet result from the interaction of these dietary components with the gut microbiome, where they selectively enrich specific microbial species and increase microbial diversity. Understanding the interaction of habitual dietary patterns on the gut microbiome will lead to rational dietary manipulation to improve human health through prevention and treatment of disease.

Keywords:

• Microbiome
• plant-rich diet
• polyphenol
• fibre
• short chain fatty acids

Introduction

Epidemiological studies have long demonstrated a strong association with increased fruit and vegetable consumption and decreased risk of chronic diseases such as cardiovascular disease, type 2 diabetes and cancer (Slavin and Lloyd 2012; Aune et al. 2017). The health promoting properties of plants go beyond the provision of basic micro- and macronutrients and are multimodal as they also contain phytochemicals that function as anti-oxidants, phytoestrogens and anti-inflammatory agents (Slavin and Lloyd 2012). In addition, over the last decade it has become clear that the consumption of plants has a significant influence on the gut microbiome and that plant-rich diets can induce the expansion of gut-resident microbes that are beneficial to human physiology and overall health (Klinder et al. 2016).

Gut microbiome

The human gut is colonised by 10¹³–10¹⁴ micro-organisms that includes bacteria, archaea, viruses and fungi. These micro-organisms and their human hosts have co-evolved and developed a symbiotic relationship where microbes now perform many critical host functions including nutrient (Rodionov et al. 2019) and drug metabolism (Wilson and Nicholson 2017), maintenance of mucosal barrier (Shi et al. 2017), immunomodulation (Zeng et al. 2019) and protection against pathogens (Ren et al. 2018). The bidirectional interactions between host and microbe have become fully integrated into human health such that dysbiosis, or microbial imbalance, results in loss of regulation of this finely tuned homeostatic system, increasing risk of intestinal inflammation (Weng et al. 2019), autoimmune diseases (Sorini et al. 2019) and neurological disorders (Tremlett et al. 2017). Many non-communicable diseases seen in the Western world, such as metabolic syndrome, type 2 diabetes and obesity, are also characterised by a loss of gut microbial diversity (Konturek et al. 2015; Santos-Marcos et al. 2019).

Approximately 2,000 gut-resident bacterial species have been identified with the dominant phyla being Firmicutes, Bacteroidetes, Actinobacteria, Proteobacteria, Fusobacteria and Verrucobacteria. Firmicutes and Bacteroidetes represent 90% of the gut microbiome (Arumugam et al. 2011; Hugon et al. 2015). Each individual person is colonised by roughly 160 species with large interindividual variability (Meadow et al. 2015). The variability is driven by host genotype, immunological responses (Hooper et al. 2012), use of antibiotics (Livanos et al. 2016), lifestyle and environment (Rothschild et al. 2018). Of these factors, habitual diet plays a major role in the microbial structure and activity (David et al. 2014).

The gut microbiome changes with age, but it is relatively stable in adulthood (Yatsunenko et al. 2012). However, dietary macronutrients can rapidly, within 2–4 days, induce shifts in microbial composition and function (David et al. 2014). These changes occur as microbes obtain energy for growth from dietary nutrients that had escaped proximal digestion and absorption. Therefore, dietary intake can influence which microbes will colonise, flourish or disappear throughout life. Studies on habitual diets demonstrated associations between dietary patterns and specific microbial communities (Wu et al. 2011), i.e. animal-based diets (typically called a “Western” diet with high amounts of animal fat and protein, and processed carbohydrates) induce decreased levels of beneficial species within the Firmicutes phyla and strains from the genus Prevotella; while levels of bile-tolerant, inflammation-associated Proteobacteria, such as Bilophila, and Bacteroides are increased (Turnbaugh 2008; Arumugam et al. 2011). This diet pattern also results in loss of bacterial diversity within the microbial community and is associated with various diseases including intestinal bowel disease and obesity (Le Chatelier et al. 2013). In contrast, plant-rich diets are associated with greater microbial diversity with a dominance of Prevotella over Bacteroides. The genus Prevotella is expanded with complex carbohydrate intake as these microbes contain specific enzymes that are capable of degrading plant fibres (Singh et al. 2017). A study published in 2018 by the American Gut project (AGP; http://americangut.org) used data collected from 11,336 healthy human participants and demonstrated that the number of unique plant species an individual consumes is associated with microbial diversity, more so than being defined as “vegan”. There was also an association with increased plant consumption and short chain fatty acid (SCFA) fermenters, specifically the species Faecalibacterium prausnitzii and strains within the genus Oscillospira were increased with the number of plant species consumed (McDonald et al. 2018). Another study performed on 1,135 subjects from a Dutch population mirrored the abovementioned results showing increased microbial diversity with fruit and vegetable consumption. Interestingly, this study also found a strong association with carbohydrate consumption and decreased microbiome diversity, with a further reduction as consumption of sugar-sweetened beverages, bread, beer etc. increased (Zhernakova et al. 2016). These studies are consistent with previous work demonstrating that plant components stimulate growth of beneficial intestinal bacterial species to promote and maintain a healthy microbial environment in large part through the fermentation of fibre to SCFAs (Tabernero et al. 2011; Padayachee et al. 2017).

Acetate, butyrate and propionate are the most abundant SCFAs and they have wide-ranging impacts on host physiology. SCFA production occurs through specialised organisms that resides in the gut and include stains such as Bacteroides, Roseburia, Bifidobacterium, Fecalibacterium, and Enterobacteria (Baxter et al. 2019). Butyrate is particularly important for gut health as it stimulates the production of mucin, antibacterial peptides and tight junction proteins and is an energy source for colonocytes (Rivière et al. 2016). These effects on gut barrier function are extremely important for health as changes in the mucosal barrier have been described in intestinal bowel disease and other inflammatory conditions (Mohajeri et al. 2018). Butyrate and propionate also function as signalling molecules by interacting with G-protein coupled receptors (e.g. GPR41) to signal to the enterocytes and immune cells. An additional function of SCFAs is to lower the colonic luminal pH to inhibit growth of pathogens such as Salmonella and Escherichia coli (Duncan et al. 2009; De Filippo et al. 2010).

Plant components and the gut microbiome

Plant components that have been extensively studied for their influence on the microbiome are plant -derived dietary fibre (also known as non-digestible polysaccharides) and polyphenols. Fibre is an important component of the human diet and has known health benefits including lowering cholesterol and improving blood glucose responses (Fuller et al. 2016). Dietary fibre as a prebiotic has specific effects on the microbial populations and its function as individual taxa have been shown to selectively metabolise discrete fibre structures (Leitch et al. 2007; Holscher 2017). Dietary fibre is comprised of both soluble and insoluble carbohydrates and includes pectin, cellulose, lignin, hemicellulose, arabinoxylan, nondigestible oligosaccharide inulin, oligofructose and resistant starch. Many of these fibre types have been shown to affect the microbiome uniquely; pectin, which make up 35% of fruit fibre cell wall, increases butyrate-producing species such as Clostridium cluster XIV (Padayachee et al. 2017; Bang et al. 2018). In a study by Baxter et al. two types of resistant starches, one from high-amylose maize seed and the other from potato tubers, and inulin, a naturally occurring polysaccharide, were compared regarding their butyrate production. The resistant starches increased butyrate, while inulin increased the relative abundance of Bifidobacteria (Baxter et al. 2019). Historically inulin was consumed at levels of 25–32 g/day, while the average American today only ingests 2–8 g/day. Food sources that contain inulin include wheat, bananas, garlic, onion, agave and chicory root. Studies using inulin as a prebiotic found increased Bifidobacterium and Faecalibacterium prausnitzii, and decreased Bilophila after inulin digestion by human volunteers (Ramirez-Farias et al. 2008; Dewulf et al. 2013; Henning et al. 2017). A comparison between apple pectin and inulin using a human colonic microbial anaerobic continuous-flow fermenter found that they were both effective in promoting prebiotic activity with anti-inflammatory effects, although apple pectin was three times more effective in promoting Bacteroides growth and overall microflora diversity than inulin, presumably reflecting the differing complexity of the two prebiotics (Chung et al. 2016). Apart from using fruit and vegetable components as prebiotics, specific beneficial bacterial species have also been used as probiotics. For example, Bifidobacteria can ferment fibre and produce the metabolites acetic acid, lactic acid, B vitamins and antibacterial molecules, making it an ideal choice for a probiotic (Holscher et al. 2015). In addition to fibre, polyphenols are also abundantly available in fruits and vegetables. Most polyphenols pass through the small intestine and can therefore influence the microbes residing in the large intestine. Polyphenols exist in various forms including flavanols, flavanones and anthocyanins (Ozdal et al. 2016). Specific bacterial strains that have the ability to process dietary polyphenols have been identified and include Eubacterium ramulus, Adlercreutiza equolifaciens and Flavonifractor plautii (Pasinetti et al. 2018).

In a whole food approach, Holscher et. al. demonstrated that walnut consumption at 42 g/day, increased butyrate-producing Clostridium clusters XIV and IV including, Faecalibacterium, Roseburia, while lowering the relative abundance of Ruminococcus, Dorea, Oscilllo, Bifidobacteria. Walnut consumption also decreased pro-inflammatory bile acids deoxycholic acid and lithocholic acid and serum LDL cholesterol (Holscher et al. 2018). A similar study performed with almonds (dose of 42 g/day) showed an increase in the relative amount of Lachnospira, Roseburia, and Dialister (Holscher et al. 2018). Also, broccoli containing both dietary fibre and glucosinolates (plant secondary metabolites) exerted a 9% decrease in Firmicutes, while causing a reciprocal increase in the phyla Bacteroidetes (Kaczmarek et al. 2019). Consumption of fruit/vegetable juice for 3 days followed by 14 days of habitual diet also reduced Firmicutes and Proteobacteria, with a significant increase in Bacteroidetes and Cyanobacteria (Henning et al. 2017). In a dietary pattern approach, a study examining the adherence to a Mediterranean diet, which is high in fruit and vegetables, and its effect on the microbiome, showed a higher Firmicutes-Bacteroidetes ratio with lower adherence to this diet. A greater presence of Bacteroidetes was associated with lower animal protein intake and adherence to the Mediterranean diet was also associated with significantly higher levels of total SCFA (Garcia-Mantrana et al. 2018).

Future perspectives

The past decade has revealed many of the roles the gut microbiome plays in human health. Health promoting strains such as Bifidobacterium, Akkermansia muciniphila, Lactobacillus and strains that are associated with negative health outcomes (i.e. Bacteroides and Ruminococcus) have been identified. We have also started to mechanistically understand the interaction between bacterial strains and their fermentation products; Faecalibacterium and Roseburia are capable of generating butyrate from acetate.

From a dietary point of view, the next critical step in understanding the role the microbiome plays in human health, is to identify how diet and food components alter the microbiome to generate metabolites that affect health outcomes. Changes in dietary intake, specifically changes in diet composition can induce acute alterations in the microbiome, but it is habitual diet that determines the long-term residents of the gut. Many studies have investigated isolated dietary components such as specific dietary fibre types used as prebiotics. However, understanding the effects of specific whole foods and diet patterns on the gut microbiome will lead to rational dietary manipulation to improve health through prevention and treatment of disease.

Disclosure statement

The author declares no conflict of interest.