Diet and lifestyle outweigh genetic background in shaping gut microbiome across nonhuman and human primates

The source of variation in the composition and function of the microbiome within and between species is yet to be fully understood. Although genetic background and diet have been suggested as major drivers of gut microbiome composition, the role of genetics versus environmental factors in driving gut microbiome variation in closely related primates remains unclear.

A new study by Dr. Andres Gomez, from the University of Minnesota (USA), and colleagues explores factors that shape gut microbiome composition across 9 different primate species and 4 human groups exposed to different subsistence patterns.

The researchers analyzed fecal samples of anthropoid primates—including African great apes, Old World monkeys and New World monkeys—and human populations made up of hunter-gatherers and traditional agriculturalists. Data from US participants in the Human Microbiome Project were also included.

Gut microbiota composition was different in the fecal samples of all the primate species analyzed. The geographical origin and subsistence strategy led to specific groups of gut microbiome profiles shared across genetically distant primates.

Specifically, African monkeys from the subfamily Cercopithecinae—including mangabeys, baboons, and vervets—whose subsistence is based on foraging had a similar gut microbiome to human groups that rely on nonindustrial dietary patterns, even though they are phylogenetically distant primates. The authors hypothesize that gut microbiome similarity between human hunter-gatherers and agriculturalists and Old World monkeys is a result of sharing a diet that shows a high diversity of nutrients consisting of multiple substrates for the microbiome, rather than depending on a single category of foods.

Western researchers living in the Central African Republic who transitioned to the lifestyle of traditional agriculturalists also showed gut microbiome trends similar to those seen in traditional agriculturalists and hunter-gatherers, which, in turn, differed from humans in the United States.

Gomez and colleagues also identified three common gut microbiome signatures in African monkeys and hunter-gatherer and agriculturalist populations. Bacterial taxa belonging to group 1—dominated by Prevotella, Coprococcus, Clostridium, Faecalibacterium, Lachnospira and unclassified members—led to a gut microbiome with the highest levels of diversity. This group was then followed by the other two.

The highest levels of gut microbiome diversity were found in monkeys and humans practicing traditional subsistence with a mixture of fermentable fibers. In contrast, primates that rely on diets with the highest content of complex fibers, such as gorillas, showed lower levels of gut microbiome diversity. These results show the importance of avoiding simplistic associations that have long been reported in the microbiome field, such as “Enterotype enriched with Prevotella – Dietary fiber, vegetables and fruits” and “Enterotype enriched with Bacteroidetes – Protein and animal fat”.

On the whole, these findings show that the human gut microbiome is highly plastic at the genus level. Contrary to previous thought, these findings highlight environmental factors as major drivers of gut microbiome composition when compared with host-species phylogenies.

Such findings show that diet may outweigh phylogenetic evolution in shaping gut microbial communities. According to the researchers: “These data support an ecological model rather than evolutionary convergence on primate gut microbiomes.”

Reference:

Gomez A, Sharma AK, Mallott EK, et al. Plasticity in the human gut microbiome defies evolutionary constraints. mSphere 4: 2019. doi: 10.1128/mSphere .00271-19.