Comparative genomics of Sphingomonas from the cupuassu (Theobroma grandiflorum) phyllosphere reveals signatures of host adaptation and beneficial interactions

Members of the genus Sphingomonas are ubiquitous phyllosphere inhabitants recognized for their metabolic versatility and intimate associations with plants. Here, we describe and compare eight high-quality metagenome-assembled genomes (MAGs) of Sphingomonas recovered from leaves of the witches’-broom–resistant cupuassu (Theobroma grandiflorum) genotype C174. These MAGs represent four known species — S. adhaesiva (bin09, bin18, bin28), S. fennica (bin11), S. phyllospherae (bin08, bin10), and S. taxi (bin15, bin20) — and one novel lineage proposed as CandidatusSphingomonascupuassunensis. Comparative analyses with 15 reference Sphingomonasgenomes revealed a conserved core of 623 orthologous protein families and extensive genomic divergence, reflecting broad adaptive plasticity within the genus. Functional annotation uncovered substantial variability in xenobiotic degradation, nitrogen metabolism, secretion systems, and carbohydrate-active enzymes. Notably, genes encoding effector-related proteins, including avrXca, were identified in S. phyllospherae (bin08, bin10) and S. adhaesiva (bin09, bin28), suggesting potential immunomodulatory interactions with the host plant. Together, these findings highlight the genomic and functional diversity of Sphingomonas inhabiting the cupuassu phyllosphere and provide an evolutionary and ecological framework to explore their roles in tropical plant–microbe symbioses and host disease resilience. Summary of the steps and methodologies used to analyze the diversity and potential of MAGs identified as belonging to the Sphingomonas genus