Diet Quality, Food Groups and Nutrients Associated with the Gut Microbiota in a Nonwestern Population

Ángela S García-Vega, Vanessa Corrales-Agudelo, Alejandro Reyes, Juan S Escobar, Ángela S García-Vega, Vanessa Corrales-Agudelo, Alejandro Reyes, Juan S Escobar

Abstract

Diet plays an important role in shaping gut microbiota. However, much remains to be learned regarding this association. We analyzed dietary intake and gut microbiota in a community-dwelling cohort of 441 Colombians. Diet quality, intake of food groups and nutrient consumption were paired with microbial diversity and composition using linear regressions, Procrustes analyses and a random-forest machine-learning algorithm. Analyses were adjusted for potential confounders, including the five cities from where the participants originated, sex (male, female), age group (18-40 and 41-62 years), BMI (lean, overweight, obese) and socioeconomic status. Microbial diversity was higher in individuals with increased intake of nutrients obtained from plant-food sources, whereas the intake of food groups and nutrients correlated with microbiota structure. Random-forest regressions identified microbial communities associated with different diet components. Two remarkable results confirmed previous expectations regarding the link between diet and microbiota: communities composed of short-chain fatty acid (SCFA) producers were more prevalent in the microbiota of individuals consuming diets rich in fiber and plant-food sources, such as fruits, vegetables and beans. In contrast, an inflammatory microbiota composed of bile-tolerant and putrefactive microorganisms along with opportunistic pathogens thrived in individuals consuming diets enriched in animal-food sources and of low quality, i.e., enriched in ultraprocessed foods and depleted in dietary fiber. This study expands our understanding of the relationship between dietary intake and gut microbiota. We provide evidence that diet is strongly associated with the gut microbial community and highlight generalizable connections between them.

Keywords: 16S rRNA; 24-h dietary recall; Colombians; community dwellers; food consumption; gut microbiome; short-chain fatty acids.

Conflict of interest statement

While engaged in this project, V.C.-A. and J.S.E. were employed by a research center that belongs to a food company (Grupo Empresarial Nutresa); A.S.G.-V. received economic stipend support from the same research center; A.R. had no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

Figures

Figure 1
Figure 1
Diet features in the studied population. (A) Heatmap showing Pearson’s product moment correlations between pairs of food groups. Dendrograms obtained by hierarchical Ward-linkage clustering. (B,C) Principal component analysis (PCA) projecting the intake of food groups on the first three components. (D) Heatmap showing Pearson’s product moment correlations between pairs of nutrients. (E,F) PCA projecting the intake of nutrients on the first three components.
Figure 2
Figure 2
Gut microbiota diversity and composition of the studied population. (A) Distribution of alpha diversity (Shannon diversity index) by sex and age group. (B) Taxonomic profile at the class level. Classes with a median relative abundance equal to zero were combined into “Other”. The color code corresponds to the taxonomic classification at the phylum level.
Figure 3
Figure 3
Heatmap showing Spearman’s correlation coefficients between operational taxonomic unit (OTU) relative abundance and diet quality. The set of OTUs associated with multivariable-adjusted diet quality indexes were obtained with a regression-based random-forest machine-learning algorithm. Dendrograms obtained by hierarchical Ward-linkage clustering. The colored branches of the dendrogram are for illustrative purposes: brown branches highlight OTUs associated with diets of high quality, while purple branches highlight OTUs associated with diets of low quality. The taxonomic classification at the class level of each OTU is noted at the left side of the heatmap. Values in parentheses next to quality indexes indicate the number of OTUs selected by the random forest. HEI = adapted Healthy Eating Index 2015; GABA = Colombian Food-Based Dietary Guidelines.
Figure 4
Figure 4
Heatmap showing Spearman’s correlation coefficients between OTU relative abundance and food-group intake. The set of OTUs associated with multivariable-adjusted food-group intake was obtained with a regression-based random-forest machine-learning algorithm. We also included the first three components of the food-group PCA. Dendrograms obtained by hierarchical Ward-linkage clustering. The colored branches of the dendrogram are for illustrative purposes: brown branches highlight OTUs associated with plant-derived food groups, while purple branches highlight OTUs associated with animal-derived food groups. The taxonomic classification at the class level of each OTU is noted at the left side of the heatmap. Values in parentheses in the x-axis indicate the number of OTUs selected by the random forest.
Figure 5
Figure 5
Associations between nutrient intake and gut microbiota. (A) Correlation between the gut microbiota alpha diversity (Shannon diversity index) and nutrient intake (regression line with 95% confidence intervals). PC2 (x-axis) provides information about the sources of nutrients: negative values indicate nutrients obtained mainly from plant-food sources, whereas positive values are associated with nutrients obtained mainly from animal-food sources. (B) Heatmap showing Spearman’s correlation coefficients between OTU relative abundance and nutrient intake. The set of OTUs associated with multivariable-adjusted nutrient intake were obtained with a regression-based random-forest machine-learning algorithm. We also included the first three components of the nutrient PCA. Dendrograms obtained by hierarchical Ward-linkage clustering. The colored branches of the dendrogram are for illustrative purposes: brown branches highlight OTUs associated with nutrients mainly obtained from plant-food sources, purple branches highlight OTUs associated with nutrients mainly obtained from animal-food sources and blue branches highlight OTUs associated with PC3 (i.e., vitamins of the B complex). The taxonomic classification at the class level of each OTU is noted on the left side of the heatmap. Values in parentheses in the x-axis indicate the number of OTUs selected by the random forest.

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