The Inuit gut microbiome is dynamic over time and shaped by traditional foods

Abstract

Background: The human gut microbiome represents a diverse microbial community that varies across individuals and populations, and is influenced by factors such as host genetics and lifestyle. Diet is a major force shaping the gut microbiome, and the effects of dietary choices on microbiome composition are well documented. However, it remains poorly known how natural temporal variation in diet can affect the microbiome. The traditional Inuit diet is primarily based on animal products, which are thought to vary seasonally according to prey availability. We previously investigated the Inuit gut microbiome sampled at a single time point, and found no detectable differences in overall microbiome community composition attributable to the traditional Inuit diet.

Results: To determine whether seasonal changes in the Inuit diet might induce more pronounced changes in the microbiome, we collected stool and toilet paper samples, and dietary information from Inuit volunteers living in Resolute Bay (Nunavut, Canada), and compared them to individuals of European descent living in Montréal (Québec, Canada) consuming a typical Western diet. We sequenced the V4 region of the 16S rRNA gene to characterize microbiome diversity and composition, and compared samples collected with toilet paper or from stool. Our results show that these sampling methods provide similar, but non-identical portraits of the microbiome. Based on toilet paper samples, we found that much of the variation in microbiome community composition could be explained by individual identity (45-61% of variation explained, depending on the beta diversity metric used), with small but significant variation (3-5%) explained by sex or geography (Nunavut or Montréal). In contrast with our previous study at one time point, sampling over the course of a year revealed that diet explains 11% of variation in community composition across all participants, and 17% of variation specifically among Nunavut participants. However, we observed no clear seasonal shifts in the microbiomes of participants from either Nunavut or Montréal. Within-individual microbial diversity fluctuated more over time in Nunavut than in Montréal, consistent with a more variable and highly individualized diet in Nunavut.

Conclusions: Together, these results shows that the traditional Inuit diet and lifestyle has an impact on the composition, diversity and stability of the Inuit gut microbiome, even if the seasonality of the diet is less pronounced than expected, perhaps due to an increasingly westernized diet.

Keywords: 16S rRNA gene; Dietary transition; Gut microbiome; Inuit traditional diet; Temporal variation; Western diet.

Fig. 1

Paired toilet paper and stool samples do not differ in richness, but differ slightly in composition. a Comparison of Shannon alpha diversity between paired stool and toilet paper samples. No significant difference in diversity was observed (paired t test, p = 0.7053). See Additional file 2 Figure S2 for additional alpha diversity measures. b Principal coordinates analysis (PCoA) of Unweighted UniFrac distances computed between paired stool and toilet paper samples from the same individual (see Additional file 2 Figure S3 for additional metrics). Each color represents a single individual and the shapes identify the sample type. A small but significant difference was observed between the community compositions of the two sample types (permanova R ² = 0.04, p = 0.0017) comparatively to a larger significant difference between paired samples (permanova R ² = 0.75, p = 0.0001)

Fig. 2

Microbiomes vary mainly by individual, and slightly by geography. Principal coordinates analysis (PCoA) of Unweigthed UniFrac distances computed between paper toilet samples (see Additional file 2 Figure S4 for additional metrics). Montréal and Nunavut microbiomes cluster by (a). geography (permanova R ² = 0.04, p = 0.0001), by (b) individual participant identity (permanova R ² = 0.45, p = 0.0001), and by sex (permanova R ² = 0.03, p = 0.0001)

Fig. 3

Variation in diet explains differences in microbial community structure between Montréal and Nunavut. a Bar chart showing the mean frequency (number of times eaten per participant ± standard deviation) of each food category over the 2 days preceding sampling. "Refined" refers to refined sugars, "Fruits and" refers to fruits and vegetables, and "Sweetened" refers to sweetened drinks. b Canonical redundancy analysis (RDA) of Unweigthed UniFrac distances calculated between all toilet paper samples from Montréal and Nunavut, with food groups as explanatory variables (adjusted R ² = 0.11, p = 0.001). Each point represents a single sample. All time points from all participants are included

Fig. 4

Greater temporal alpha and beta diversity variation within individuals in Nunavut. a Distribution of dispersion in alpha diversity over time for each individual participant who contributed at least three samples. Dispersion is here defined as the absolute difference in Shannon diversity in each sample from the mean Shannon diversity for a particular individual. The participants from Nunavut have significantly higher alpha diversity dispersion over time than participants from Montréal (permutational t test, p = 0.0061). b Distribution of dispersion in beta diversity over time within the same participants. Dispersion is here defined as the distance of each sample to the centroid for that individual in compositional space, using unweighted UniFrac distances. The participants from Nunavut have significantly higher dispersion in beta diversity over time than participants from Montréal (permutational t test, p = 0.0124)