The Edible Plant Microbiome represents a diverse genetic reservoir with functional potential in the human host

Maria J Soto-Giron,Jillian Dewalt,Tracy J Mincer,Thomas Ishoey,Claudine Tahmin,Eric Schott,Ji-Nu Kim,Gerardo Toledo

doi:10.1038/s41598-021-03334-4

Abstract

Plant microbiomes have been extensively studied for their agricultural relevance on growth promotion and pathogenesis, but little is known about their role as part of the diet when fresh fruits and vegetables are consumed raw. Most studies describing these communities are based on 16S rRNA gene amplicon surveys, limiting our understanding of the taxonomic resolution at the species level and functional capabilities. In this study, we characterized microbes colonizing tomatoes, spinach, brined olives, and dried figs using shotgun metagenomics. We recovered metagenome-assembled genomes of novel lactic acid bacteria from green olives and identified high intra- and inter-specific diversity of Pseudomonas in tomatoes. All samples were colonized by Pseudomonas, consistent with other reports with distinct community structure. Functional characterization showed the presence of enzymes involved in vitamin and short chain fatty acid metabolism and degradation of diverse carbohydrate substrates including plant fibers. The dominant bacterial members were isolated, sequenced, and mapped to its metagenome confirming their identity and indicating the microbiota is culturable. Our results reveal high genetic diversity, previously uncultured genera, and specific functions reflecting a likely plant host association. This study highlights the potential that plant microbes can play when consumed as part of our diet and proposes these as transient contributors to the gut microbiome.

Highlights

Some metabolites such as plant hormones produced in concert with the plant microbiome can be relevant in the human g ut[9], suggesting a co-adaptation to colonize both the plant and animal host
Comparison of sequence diversity based on metagenomic reads with other metagenomes from different environments showed that samples from this study present similar diversity to the ones seen in the human stool and slightly higher than Nunu, a west African fermented yogurt-like milk product, but lower than marine, fresh water, and soil samples (Fig. 1A)
Together with the Edible Plant Microbiome concept previously described by Berg et al.[5], we were interested in characterizing the diversity and functional capabilities of the Edible Plant Microbiome in common dietary fruits and vegetables

Summary

Introduction

Some metabolites such as plant hormones produced in concert with the plant microbiome can be relevant in the human g ut[9], suggesting a co-adaptation to colonize both the plant and animal host. The consumption of raw fruits and vegetables in salads is considered healthy and provides abundant and diverse microorganisms that may be functionally active along the passage through the GI tract of the consumer Fermented foods are another dietary component rich in microbes. Cernava et al.[22] analyzed the arugula phyllosphere and reported the resistome as part of the gene content with ecological significance These types of analyses are useful to describe the microbial diversity and the linkage with metabolic pathways associated with plant fiber degradation, vitamin biosynthesis, and short chain fatty acid metabolism in plant-associated microbiomes. Our results suggest the Edible Plant Microbiome is a functional component of the diet that might contribute to the gut microbiome with potential implications for human nutrition and health

Methods

Results

Conclusion