Microbiome analysis uncovers fruit-specific microbial community divergence between wild and cultivated watermelon varieties

Domestication not only modulates the genetic characteristics of crops but also reconfigures their associated microbial communities, which subsequently impact plant health, disease resistance, and ecological adaptability. In our study, we explore the disparities in microbial communities, metabolic profiles, and fruit quality between the domesticated watermelon cultivar <italic>Citrullus lanatus</italic> var. <italic>vulgaris</italic> (M1511-3) and its wild progenitor, <italic>Citrullus mucosospermus</italic> (PI595203). Our findings reveal that domestication profoundly reshapes microbial composition: <italic>Citrullus lanatus</italic> var. <italic>vulgaris</italic> (M1511-3) is predominantly colonized by <italic>Sphingomonas</italic> species, which facilitate fruit development and enhance sweetness, whereas <italic>Citrullus mucosospermus</italic> (PI595203) sustains a more diverse microbial community, encompassing Gammaproteobacteria, <italic>Bacilli</italic>, and <italic>Actinomycetia</italic>, which confer increased ecological resilience and disease resistance. These microbial discrepancies are reflected in divergent metabolic profiles: <italic>Citrullus mucosospermus</italic> (PI595203) exhibits enhanced nucleotide and D-amino acid metabolism, indicative of superior stress adaptation, whereas <italic>Citrullus lanatus</italic> var. <italic>vulgaris</italic> (M1511-3) demonstrates optimized carbohydrate, lipid, and amino acid metabolism, underpinning its superior fruit quality. Furthermore, the microbial community of <italic>Citrullus lanatus</italic> var. <italic>vulgaris</italic> (M1511-3) exhibits augmented redox and carbohydrate-binding capacities, while <italic>Citrullus mucosospermus</italic> (PI595203) displays a broader enzymatic repertoire, promoting more efficient carbohydrate utilization and enhanced environmental adaptability. Remarkably, <italic>Citrullus mucosospermus</italic> (PI595203) harbors approximately 40 antibiotic resistance genes, underscoring its ability to withstand pathogen-induced stress. In contrast, <italic>Citrullus lanatus</italic> var. <italic>vulgaris</italic> (M1511-3) leverages optimized metabolic pathways to enhance fruit quality. These findings emphasize the pivotal role of microbial interactions in shaping plant traits and suggest the potential of introducing beneficial microbes, such as <italic>Sphingomonas</italic>, to enhance crop resilience and quality.