From green to red: metabolic reprogramming and bacterial community succession underpin cherry tomato fruit ripening and quality formation

Tomato fruit ripening is accompanied by profound biochemical and microbial-associated changes that collectively shape fruit flavor, quality, and susceptibility to (a)biotic stresses. However, integrated insights into the co-varying effect of metabolic reprogramming and fruit-associated microbiome across ripening stages remain limited. Here, we employed a multi-omics approach to investigate stage-dependent shifts in the metabolome and bacteriome of cherry tomato fruits across three ripening stages: mature green, pink, and red ripe. Fruit quality analysis revealed a significant increase in soluble sugars, lycopene, and ascorbic acid from the green to the red stage. Untargeted metabolomics showed extensive metabolic reprogramming during ripening, characterized by the marked accumulation of lipids, amino acids, carbohydrates, terpenoids, and flavonoids in red ripe fruits, alongside a decline in defensive alkaloids such as tomatine. High-throughput 16S rRNA amplicon sequencing showed that bacterial diversity and community composition shifted significantly with ripening, with red ripe fruits harboring higher diversity and enrichment of gram-positive taxa, including Bacillus , Clostridium , Enterococcus , Lactiplantibacillus , Litchfieldia , and Pediococcus , whereas Pseudomonas was enriched in the mature green stage. Correlation analysis revealed a strong association between specific bacterial taxa and ripening-related metabolites, suggesting a link between microbial succession and metabolic remodeling. Together, these findings demonstrate that tomato fruit ripening involves tightly coupled metabolic and microbial dynamics, providing new insights into fruit quality formation and postharvest ecology for sustainable agriculture.