Empty calories: full of conflict?

Helen Wasielewski and Athena Aktipis and I recently published “Resource conflict and cooperation between human host and gut microbiota: implications for nutrition and health” in Annals of the New York Academy of Sciences.

We explored the idea that that human fitness is not always be perfectly aligned with the fitness interests of our microbes. We proposed that those conflicts of interest underlie the association between the Western diet and chronic diseases. Foods that make up the Western diet might agitate conflict and reduce cooperation between human and resident microbiota.

It has been popular to characterize the microbes inhabiting our bodies as mutualists, beneficial organisms that are vital for the healthy functioning of the body. While mutually beneficial cooperation does occur in the gut, so does conflict. Bacteria are also capable of complex behaviors, potentially changing from benign to deadly. Interactions between human and microbe therefore have the potential to benefit both partners, harm both, or help one partner at the expense of the other, (just like interactions between different humans!) The outcome of these interactions often depends on the diet.

Is cheap ice cream a conflict food?

Some common food additives select for microbes and microbial behaviors that worsen conflict between human and microbiota. For example, emulsifiers, such as polysorbate-80 and carboxymethylcellulose, are commonly added to ice cream and other foods to improve their texture. Maltodextrin is a commonly used thickener. Unfortunately these emulsifiers and thickeners also erode the mucus barrier of the gut, exacerbating conflicts between microbe and host over the suitability of host habitat for colonization.

Emulsifiers increase microbe adhesion to epithelial cells, a precursor to tissue invasion

Other nutrients agitate conflict by giving advantages to organisms with fitness interests that are not aligned with the host’s fitness interests. These foods serve as growth substrates for pathogens and pathobionts (potentially harmful microbes).

Iron is a conflict food

Dietary iron can exacerbate conflict between host and pathogens.

Excess iron advantages pathogens, altering the microbiome in favor of harmful microbes, provoking inflammation and conflict with the host.

Sugar is a conflict food.

Simple carbohydrate, like sugar, is an energy source that can be exploited by host and harmful microbe alike. Our guts have evolved to absorb simple carbohydrates quickly in the proximal gut, where most microbial competitors are kept out, (for instance with acid, bile, and antimicrobial peptides). The high sugar content of the Western diet overwhelms these antimicrobial functions, potentially fueling harmful ecological changes in the gut.

Humans use low pH to keep competitors at bay. Sugar & fats are absorbed where microbe density is low

Low fiber foods are conflict foods.

The Western diet, with easily accessible carbohydrates and low in fiber, erodes the mucus layer, and increases pathogen and pathobiont growth and adhesion to the intestinal epithelium. These low fiber foods select for microbes and functions in conflict with the interests of the host.

Host microbiome conflicts may cause undesired weight gain?

Which foods feed cooperation in the gut?

Foods that selectively feed fitness enhancing microbes tend to cultivate cooperation between host and microbiome. Human milk oligosaccharides (HMO) are nutrients that evolved to feed specific strains of Bifidobacteria that protect infants. This mutualism requires provision of nutrients that are relatively inaccessible to pathogens. HMO in breast milk fits the bill.

Intestinal cells directly provision carbohydrates to microbes – an example of cooperation?

Fucosyllated carbohydrates on intestinal epithelial cells

O-glycosylated carbohydrates, secreted directly by human gut epithelial cells, are also relatively inaccessible to pathogens. These resource transfers from host to microbe may encourage the growth of mutualists that protect us from infection.

Dietary fiber is also relatively inaccessible to harmful microbes and tends to promote cooperative behaviors:

Other foods that may favor cooperation include marine oils, polyphenols, and flavonoids. These nutrients have anti-pathogen effects that synergize with the immune system – but we will save this discussion for a later post.

The open access text of Wasielewski Alcock and Aktipis NYAS (2016) is available here.

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Joe Alcock

Emergency Physician, Educator, Researcher, interested in the microbiome, evolution, and medicine