Nomadic Irish Travellers’ gut microbiome is shaped by housing conditions rather than diet and can be seen as an indicator of cultural transition

Exploring human-microbial interactions from an evolutionary angle is important for understanding, preventing and treating ‘modern’ immune and metabolic diseases on the rise worldwide. Due to the accelerated changes in diets and lifestyles in urban societies compared to traditional societies, scientists have shown an increasing interest in studying the gut microbiome of non-industrialized societies to characterize human biological adaptations to changing lifestyles.

The diversity of bacteria and viruses in small isolated human populations may be perturbed by industrialization, with an impact on health that we are only just beginning to understand. For instance, the gut microbiomes of pre-agricultural Hadza, Inuit and Papua New Guinean societies have bacterial families that are rare or absent in the microbiota of industrialized nations. In contrast, agricultural and westernized groups exhibit an increase in sugar and xenobiotic processing, coupled with a loss of enzymes involved in degrading certain types of plants.

The diversity of bacteria and viruses in small isolated human populations may be perturbed by industrialization, with an impact on health that we are only just beginning to understand

A new study of a marginalized Irish community transitioning from a traditional nomadic lifestyle to conventional housing increases understanding of diet and lifestyle factors that shape the gut microbiome.

Irish Travellers are an ethnic minority in Ireland that began to form as a distinct and separate population between 200 and 1,200 years ago. As a result, the traditional Irish Traveller community is isolated from the broader Irish community, lives in large families, and exists in close proximity to dogs and horses as both companions and work animals.

Since 2002, however, the Irish Traveller community is experiencing a lifestyle transition due to legislation that forced its members to move into state-sponsored housing or so-called “halting sites”.

Keohane and colleagues collected stool samples from 118 adult Irish Travellers and compared them with both the gut microbiomes of people in the same geographic locality and that of people in other industrialized and non-industrialized countries, available from public datasets. Most members of the Irish Traveller community under study were nomadic as children, while they adopted a more settled lifestyle later, were vaginally delivered, were fed formula, lived within a family of 10 children, cohoused with pets or other domesticated animals, and showed a low presence of autoimmune diseases (e.g., the incidence of inflammatory bowel disease was unusual).

The gut microbiome of the Irish Travellers was classed as being somewhere between that of industrialized populations and that of non-industrialized populations. Within this intermediate Traveller gut microbiome, three groups were observed: industrial-like, non-industrial-like and intermediate. Some differences were reported when comparing them with other non-industrialized groups (indigenous, rural-dwelling hunter-gatherers from Fiji, Madagascar, Mongolia, Peru and Tanzania). In particular, Treponema was enriched in the gut microbiome of non-industrialized populations but not in that of the Irish Travellers.

The authors were also interested in disentangling which dietary or lifestyle factors might explain the gradient of gut microbiomes among the Travellers’ transitioning population. By using a machine-learning approach informed by 25 lifestyle factors, they found that lifestyle factors (especially housing conditions) outweighed diet in driving the Traveller microbiome’s transition. The factors showing the dominant influence included (ordered from highest to lowest significance): housing conditions, number of siblings, perceived well-being (as assessed by the World Health Organization Well-Being Index), pet ownership, body mass index, age, alcohol consumption, and gender. The lifestyle transition to a halting site—with its high degree of communal living with other people and animals—resulted in a non-industrialized-like microbiome, whereas transition to a house most often resulted in an industrialized-Like microbiome.

The metagenomic analysis of stool samples showed that the subgroup with an industrialized-like microbiome had an increased predicted capacity for degrading animal-derived carbohydrates and mucin; a depleted expression of metabolic pathways involved in butyrate production; and increased production of trimethylamine compared to their non-industrialized-like counterparts. Strikingly, those features were not related to the Travellers’ dietary patterns, which are high in fat and protein, suggesting other environmental factors are involved, which, in turn, deserve further characterization.

Altogether, the observed functional changes linked to industrialization may predispose Travellers to chronic diseases, although the authors did not explore to what extent the composition and functional microbiome differences observed were related to health outcomes.

In the light of the observed changes in the gut microbiome, Keohane and colleagues suggest that the absence of inflammatory bowel diseases among the Traveller community—as reported by participants’ family history—might be linked to the environment in which they live.

The observed functional changes linked to industrialization may predispose Travellers to chronic diseases

Similarly, a 2016 study found that the children of two genetically similar communities show different rates of asthma. On comparing the Amish, who practice traditional farming, live on single-family dairy farms and rely on horses for fieldwork and transportation, with the Hutterites, who live on highly industrialized and large communal farms, the study’s findings suggested about 5% of Amish children have asthma, compared to 21% of Hutterite children. While the authors did not measure the gut microbiome, the Amish children were shown to have more anti-inflammatory innate immune cells, attributed to higher microbial exposure and assessed by the microbiome composition of indoor dust samples.

The findings reiterate that genes alone do not determine future outcomes. Chronic diseases may emerge from the dance between genes and the environment and, in that regard, changes in the gut microbiome secondary to urbanization—such as the acute lifestyle transition studied here—might offer a potential target for lifestyle-related interventions that tackle the rapid rise in modern health diseases. However, in disease-centered microbiome science, it is important to keep in mind that anthropology, ecology, and evolutionary studies are also needed to improve our understanding of the impact of human microbiome on health, as the microbial anthropologist Maria Gloria Dominguez-Bello acknowledged in a 2016 story in Cell that still remains valid today.

References:

 Dominguez-Bello MG, Godoy-Vitorino F, Knight R, Blaser MJ. Role of the microbiome in human development. Gut. 2019; 68(6):1108-1114. doi: 10.1136/gutjnl-2018-317503.

Keohane DM, Shankar Ghosh T, Jeffery IB, et al. Microbiome and health implications for ethnic minorities after enforced lifestyle changes. Nat Med. 2020. doi: 10.1038/s41591-020-0963-8.

Devkota S. The gut microbiome during acute lifestyle transition. Nat Med. 2020. doi: 10.1038/s41591-020-0980-7.

Stein MM, Hrusch CL, Gozdz J, et al. Innate immunity and asthma risk in Amish and Hutterite farm children. N Engl J Med. 2016; 375(5):411-421. doi: 10.1056/NEJMoa1508749.

Dominguez-Bello MG. A microbial anthropologist in the jungle. Cell. 2016; 167(3):588-594. doi: 10.1016/j.cell.2016.09.047.