Desert Cucurbit Microbiomes: Spatiotemporal Dynamics and Functional Adaptations

Abstract

BackgroundPlant microbiomes can contribute to host adaptation in extreme environments, particularly deserts where high temperatures, intense radiation, water limitation, and nutrient-poor soils constrain plant survival. Citrullus colocynthis is a desert-adapted cucurbit with medicinal and agricultural relevance, yet integrated understanding of its microbiome across seasons, tissues, habitats, and functional traits remains limited. Here, we asked whether spatiotemporal microbiome dynamics in C. colocynthis are linked to microbial functional potential and cultivable traits relevant to persistence under arid conditions. ResultsTo address this, we profiled the microbiome of C. colocynthis across two sites, two seasons, and multiple compartments using 16S rRNA amplicon screening, shotgun metagenomics, culture-based phenotyping, and genome analysis. Amplicon profiling provided an exploratory framework and showed that plant-associated bacterial communities were shaped primarily by season and tissue type, with roots emerging as the most season-responsive compartment. Shotgun metagenomics confirmed stronger seasonal restructuring in root bacterial communities than in leaves and extended taxonomic profiling to fungal and archaeal fractions, which were interpreted descriptively because of low read representation. Summer root communities were enriched in actinobacterial genera, including Saccharopolyspora, Amycolatopsis, Pseudonocardia, and Nonomuraea, while functional profiling indicated coordinated shifts in central metabolism, cofactor salvage, exopolysaccharide-related pathways, and redox-associated functions. Twenty-four cultured bacterial isolates exhibited diverse stress-tolerance and plant growth-promoting traits, and whole-genome analyses identified biosynthetic, osmoprotective, oxidative-stress, and phytohormone-related gene content. Pangenome analysis of Pseudomonas orientalis revealed an open pangenome and lifestyle-associated accessory genes linked to host-associated functions. ConclusionsTogether, these findings connect seasonal bacterial community turnover, metagenomic functional potential, and cultivable microbial traits in a desert plant holobiont, highlighting desert-native bacteria and pathways relevant to microbiome-guided strategies for arid agriculture.