Holobiont nutrition: considering the role of the gastrointestinal microbiota in the health benefits of whole grains

Abstract

Intake of whole grains and other food products high in dietary fiber have long been linked to the prevention of chronic diseases associated with inflammation. A contribution of the gastrointestinal microbiota to these effects has been suggested, but little is known on how whole grains interact with gut bacteria. We have recently published the first human trial that made use of next-generation sequencing to determine the effect of whole grains (whole grain barley, brown rice or a mixture of the two) on fecal microbiota structure and tested for associations between the gut microbiota and blood markers of inflammation, glucose and lipid metabolism. Our study revealed that whole grains impacted gut microbial ecology by increasing microbial diversity and inducing compositional alterations, some of which are considered to have beneficial effects on the host. Interestingly, whole grains, and in particular the combination of whole grain barley and brown rice, caused a reduction in plasma interleukin-6 (IL-6), which was linked to compositional features of the gut microbiota. Therefore, the study provided evidence that a short-term increased intake of whole grains led to compositional alterations of the gut microbiota that coincided with improvements in systemic inflammation. In this addendum, we summarize the findings of the study and provide a perspective on the importance of regarding humans as holobionts when considering the health effects of dietary strategies.

Keywords: gut microbiota; inflammation; metabolic disorders; whole grains.

Figure 1. Carbohydrate composition of the whole grains used in the study and trial design. Twenty-eight subjects participated in a randomized 17-week crossover study that investigated the impact of brown rice (BR), whole-grain barley (WGB) and a combination of the two on gut microbiota composition and metabolic and immunological markers. Stool samples and blood samples (indicated by red arrows) were collected during the baseline and at the end of each treatment period.

Figure 2. Effect of whole grains on the fecal microbiota in relation to bacterial taxa linked to enterotypes. Impact of dietary treatments on the abundance of Bacteroides based on whether the subject harbored (A) the enterotype dominated by Bacteroides or (B) the other non-Bacteroides two enterotypes (Ruminococcus and Prevotella) at baseline. The abundance of the genera (C)Bacteroides and (D)Prevotella in fecal samples of all subjects throughout the treatments. Dots represent populations within individual fecal samples, color-coded according to enterotypes (green = Bacteroides-dominant, red = Ruminococcus-dominant, yellow = Prevotella-dominant). Samples of subjects that showed changes in enterotype identity are linked with lines.

Figure 3. Schematic summary depicting possible mechanisms by which whole grains influence the human host and the gut microbiota (see text for details). Red arrows indicate findings obtained in the study, and black arrows indicate hypothetical changes.