Seasonal variation in human gut microbiome composition

Abstract

The composition of the human gut microbiome is influenced by many environmental factors. Diet is thought to be one of the most important determinants, though we have limited understanding of the extent to which dietary fluctuations alter variation in the gut microbiome between individuals. In this study, we examined variation in gut microbiome composition between winter and summer over the course of one year in 60 members of a founder population, the Hutterites. Because of their communal lifestyle, Hutterite diets are similar across individuals and remarkably stable throughout the year, with the exception that fresh produce is primarily served during the summer and autumn months. Our data indicate that despite overall gut microbiome stability within individuals over time, there are consistent and significant population-wide shifts in microbiome composition across seasons. We found seasonal differences in both (i) the abundance of particular taxa (false discovery rate <0.05), including highly abundant phyla Bacteroidetes and Firmicutes, and (ii) overall gut microbiome diversity (by Shannon diversity; P = 0.001). It is likely that the dietary fluctuations between seasons with respect to produce availability explain, at least in part, these differences in microbiome composition. For example, high levels of produce containing complex carbohydrates consumed during the summer months might explain increased abundance of Bacteroidetes, which contain complex carbohydrate digesters, and decreased levels of Actinobacteria, which have been negatively correlated to fiber content in food questionnaires. Our observations demonstrate the plastic nature of the human gut microbiome in response to variation in diet.

Figure 1. Correlation of microbiome composition between replicates, individuals, and over time.

Boxplots of pairwise Spearman correlation (y-axis) of bacterial abundance is shown for data at each taxonomic level (x-axis) across different classification levels. ‘Replicates’ refer to technical replicates derived from separate DNA extractions and library preparations from the same sample.

Figure 2. Consistent temporal shifts observed in microbiome composition.

Principal components analysis (PCA) of data obtained from samples collected in the summer (red triangle) and winter (blue circle), at the phylum (A), class (B), order (C), family (D), and genus (E) level across samples. F) Individual shifts in microbiome composition along PC1 (y-axis). Data from the same individual across seasons is connected by a line (gray lines represent individuals showing seasonal trend, black lines highlight individuals showing the opposite trend). G) The average pairwise distance along the PC1/PC2 plane is shorter where points are from the same season than points between seasons (t-test P = 3.38×10⁻⁷⁸), supporting seasonal clustering along the first two principle components.

Figure 3. Phylum level taxa abundances differ by season.

A) Abundance (y-axis) of the 25 bacterial phyla that were detected (only the most common bacteria are indicated in the legend) by individual (x-axis). Individual's order along the x-axis is identical in both panels. Phyla that are significantly differentially abundant between seasons (FDR <0.05) are indicated by an asterisk. B) Examples of three common phyla whose abundances (y-axis) are significantly different across seasons (x-axis): Firmicutes (q-value<0.002), Bacteroidetes (q-value<0.002), and Actinobacteria (q-value<0.002).

Figure 4. Diversity between seasons, sexes, and age.

A) A significant difference (paired t-test P<0.002) in Shannon diversity (H′, y-axis), between season (x-axis). B) H′ between sexes is not significantly different in either winter (t-test P = 0.46) or summer (P = 0.38). C) Diversity significantly decreases with age based on the data collected from winter samples (r² = 0.1267, P<0.006), but not based on the data collected from the summer samples (r² = 0.01653, P = 0.33).

Figure 5. Produce consumption varies by season.

In summer, when fruits and vegetables are grown in colony gardens, consumption of fresh produce is higher than in winter. Conversely, when fresh produce is not as available, a higher proportion of canned or frozen fruits and vegetables are eaten. Bars indicate standard error measurements. *** P<0.001 (t-test, adjusted for multiple tests using Benjamin Hochberg correction). See Table S6 for a list of all tests performed.