The food-gut axis: the phyllosphere virome of fresh vegetables is diverse, abundant, and transmitted to the human gut virome

Abstract

Fresh vegetables harbor diverse microorganisms on leaf surfaces, yet their viral communities remain unexplored. We investigated the diversity and ecology of phyllosphere viromes of six leafy green vegetables using virus-like particle (VLP) enrichment and shotgun metagenome sequencing. On average, 9.2 x 107 viruses were present per gram of leaf tissue. The majority (93.1 {+/-} 6.2%) of these viruses were taxonomically unclassified. Virome compositions were distinct among vegetable types and exhibited temporal variations. Virulent phages with replication-enhancing auxiliary metabolic genes (AMGs) were more dominant than temperate phages with host fitness-benefiting AMGs. Analysis of 1,498 human fecal VLP metagenomes revealed that approximately 10% of vegetable viruses were present in the human gut virome, including viruses commonly observed in multiple studies. These gut-associated vegetable viruses were enriched with short-term vegetable intake, and depleted in individuals with metabolic and immunologic disorders. Overall, this study elucidates the ecological contribution of the fresh vegetable virome to human gut virome diversity.