The edible plant microbiome: evidence for the occurrence of fruit and vegetable bacteria in the human gut

Abstract

Diversity of the gut microbiota is crucial for human health. However, whether fruit and vegetable associated bacteria contribute to overall gut bacterial diversity is still unknown. We reconstructed metagenome-assembled genomes from 156 fruit and vegetable metagenomes to investigate the prevalence of associated bacteria in 2,426 publicly available gut metagenomes. The microbiomes of fresh fruits and vegetables and the human gut are represented by members in common such as Enterobacterales, Burkholderiales, and Lactobacillales. Exposure to bacteria via fruit and vegetable consumption potentially has a beneficial impact on the functional diversity of gut microbiota particularly due to the presence of putative health-promoting genes for the production of vitamin and short-chain fatty acids. In the human gut, they were consistently present, although at a low abundance, approx. 2.2%. Host age, vegetable consumption frequency, and the diversity of plants consumed were drivers favoring a higher proportion. Overall, these results provide one of the primary links between the human microbiome and the environmental microbiome. This study revealed evidence that fruit and vegetable-derived microbes could be found in the human gut and contribute to gut microbiome diversity.

Keywords: Plant microbiome; and vegetable; fruit; gut microbiome; metagenome-assembled genomes.

Figure 1.

Overview of the bioinformatic workflow for the recovery of metagenome-assembled genomes (MAGs) from fruits and vegetables and the detection of their presence in the gut. Using a total of 2,426 human gut metagenomes, this study attempted to address three research questions Q1 - can we detect fruit and vegetable associated bacteria in the human gut? Q2 - do fruit and vegetable associated bacteria persist in the human gut? Q3 - what are factors influencing fruit and vegetable associated bacteria in the human gut?

Figure 2.

Taxonomical classification of plant and human-associated bacteria and their abundance in the human gut. Phylogenetic tree showing the taxonomical classification of fruit and vegetable and human gut-associated bacteria (a). Different colors in ring 1 (R1) indicate bacterial taxonomy and ring 2 (R2) indicates the origin of the MAGs. Relative abundance of fruit and vegetable associated bacteria and their abundance in children (b) and adults (c). Bar chart showing the relative abundance of fruit and vegetable associated bacterial composition at order level in the human gut (d). Relative abundance of fruit and vegetable associated bacteria was obtained by using datasets that contained reads that only mapped to fruit and vegetable associated bacterial genomes. Different colors represent different order-level classifications. Less abundant bacterial orders were included in “others”.

Figure 3.

Contribution of fruit and vegetable associated bacteria to the diversity of the human gut microbiome. The box plots include the observed human gut-associated bacteria (a) and fruit and vegetable associated bacteria (b) based on the observed MAGs in the gut. The Kruskal-Wallis test followed by pairwise comparison at P < 0.05) within different host ages are indicated by different letters above the boxplot. The scatter plot shows the ratio of the observed fruit and vegetable associated and human gut-associated bacterial metagenome-assembled genomes (MAGs) along the age gradient (c). Community clustering of fruit and vegetable associated bacteria in the human gut is shown using a two-dimensional PCoA plot and based on a Bray–Curtis dissimilarity matrix (d). LEfSe analysis indicated fruit and vegetable associated bacterial MAGs that are enriched in different age groups (e).

Figure 4.

Impact of vegetable consumption frequency, fruit consumption frequency, and diversity of consumed plants in a week on the number of observed fruit and vegetable associated bacteria and overall heterogeneity in fruit and vegetable bacterial community composition. The box plots show the observed fruit and vegetable associated MAGs in the gut (a-c). The additional plots show the overall heterogenicity in fruit and vegetable associated MAG composition in the gut (d-f).