BackgroundIn China, decline disease with unknown etiology appeared as an epidemic among bayberry trees in the southern area of the Yangtze River. Furthermore, the use of beneficial microbes has been reported to be able to reduce the incidence of this disease, emphasizing the association of this disease with microorganisms. Therefore, it has become critical to uncover the microbiome’s function and related metabolites in remodeling the immunity of bayberry trees under biotic or abiotic stresses.ResultsThe amplicon sequencing data revealed that decline disease significantly altered bacterial and fungal communities, and their metabolites in the four distinct niches, especially in the rhizosphere soils and roots. Furthermore, the microbial communities in the four niches correlated with the metabolites of the corresponding niches of bayberry plants, and the fungal and bacterial networks of healthy trees were shown to be more complex than those of diseased trees. In addition, the role of microbiome in the resistance of bayberry trees to the occurrence of decline disease was justified by the isolation, identification, and characterization of important microorganisms such as significantly enriched Bacillus ASV804, Pseudomonas ASV815 in healthy plants, and significantly enriched Stenotrophomonas ASV719 in diseased plants.ConclusionOverall, our study revealed that the occurrence of decline disease altered the microbiome and its metabolites in four ecological niches in particular rhizosphere soils and roots of bayberry, which provides new insight into the control of bayberry decline disease.