Cell research into a North American Northern Plains tribe’s gut biota shows that the living things inside them (the bacteria, archaea, and other microbes responsible for mood, digestion, immunity, and a host of other things) are in transition. More than a century after their encounters with (and relocations by) European settlers, their guts are halfway between those seen in industrialized populations and those seen in indigenous groups around the world:
Summary
The human gut is shaped by environmental factors, producing distinct microbial communities. Indigenous individuals practicing traditional lifestyles often harbor more diverse microbiota, with taxa often absent in industrialized people. However, little engagement has occurred with American Indian communities in North America who experienced forced relocation and dietary programs during colonization. Here, shotgun metagenomics profiled the gut microbiome of people from a Northern Plains tribe (NPT) reservation in comparison to 12 global populations engaged in traditional, agrarian, or industrialized lifestyles. Analysis of the 532 samples revealed that the NPT microbiota exhibited greater bacterial and archaeal diversity than industrialized populations but reduced diversity compared to global traditional and agrarian populations. Relative to the general United States population, NPT microbiomes encoded more virulence factor and microbial defense genes and fewer CAZyme-encoding genes. These findings suggest that the NPT gut microbiome is in transition between lifestyles associated with global Indigenous and industrialized populations.…
Here, we profiled the gut microbiome of individuals from a Northern Plains tribe (NPT) reservation community. Comparison to 12 different global populations found that NPT individuals had a distinct microbial signature from other traditional, agrarian, and industrialized populations. NPT individuals harbored more microbial taxa than industrialized populations, with a greater representation of more rare phyla and species, but less diverse and fewer taxa than traditional and agrarian populations. Many classical “pathobionts” were more prevalent among NPT microbiota when compared to the United States (US) general population, despite individuals being healthy adults. Yet, the US general population microbiome encoded higher frequencies of CAZymes, which are typically associated with Indigenous populations, than in NPT microbiomes. This contributes to a unique NPT microbiome relative to non-Indigenous people in the US, which may limit generalizations of “healthy” and “diseased” microbiomes determined for majority of populations to other groups in the same geographic region and provides additional insight into microbial resilience in the gut despite the influence of industrialization.
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This work was built on a decades-long relationship between the authors and the participating community. Importantly, the corresponding author was invited to initiate this work at the request of entities within the community and performed all sample collection, sample processing, and data analysis in partnership with individuals on site, including training individuals from our partner community in approaches used here.
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Discussion
The gut microbiota of humans is influenced by multiple factors of host physiology, lifestyle, and the environment.52,53,54,55 People in the NPT are uniquely situated through their continued practice of traditional lifeways combined with the adoption of certain aspects of large-scale agrarian and industrialized life that distinguishes them from the broader US population and over half of the global population that reside primarily in urban settings and engage exclusively in industrialized lifestyles. Taxonomic profiling revealed bacterial and archaeal compositions of NPT people reside between populations with industrialized and non-industrialized lifestyles. In general, the NPT population had less diverse gut microbiota than traditional and agrarian populations. Yet, the NPT microbiota were composed of more taxa and greater microbial diversity than the surrounding US general population and other industrialized populations for some taxonomical comparisons. Greater microbial diversity compared to the US general population did not necessarily result in a detectable level of more gene diversity. Microbes found in the US general population encoded higher numbers of CAZymes relative to NPT individuals but had a reduced abundance of defense mechanisms for viral and microbial competitors. Thus, the gut microbiota identified in NPT people are distinct from that in the other global populations analyzed here and may result from a combination of environmental and lifestyle factors that are common to reservation communities in North America.…
It is unclear what factors are leading to this mosaic state, but we speculate that patterns of colonization that affect dietary patterns, environmental exposures, and place-based cultural practices likely play a role.19,35,58 For example, harvesting traditional foods like prairie turnips and fish is still practiced by many individuals, but agricultural and processed foods sold in gas stations, grocery stores, and through federal food programs dominate the diets of many individuals.59
Compared to industrialized populations, we observed a higher prevalence of classical pathogens and pathobionts among the gut microbiota of NPT individuals. It is important to note that definitions of pathogenic potential for many microbes are centered within industrialized contexts that often fail to acknowledge that the absence of these species may negatively impact health.…
In conclusion, the NPT have a distinct microbial signature in the gut compared to global traditional, agrarian, and industrialized populations that suggests a transitional state between a non-industrialized and industrialized state. Associations between environmental exposures common to reservation communities in the Northern Plains and specific gene signatures suggest that microbiota of Indigenous people may be substantially shaped by their surroundings that could also promote greater microbial diversity. Lastly, we would like to highlight the importance of working alongside of community members in production of biological datasets to address questions of interest and importance in the partner community. Strong ethical research relationships improve the contextualized understanding of results through discussion and reinforce data sovereignty.