Effects of Salinity on Assembly Characteristics and Function of Microbial Communities in the Phyllosphere and Rhizosphere of Salt-Tolerant Avicennia marina Mangrove Species

Avicennia marina is a pioneer salt-tolerant plant in coastal intertidal mangroves, an efficient blue carbon ecosystem. It is of great importance to explore how salinity affects the phyllosphere and rhizosphere microbial communities of A. marina. This study showed that the microbial communities in the phyllosphere and rhizosphere of A. marina had different constitutive properties, adaptive network interactions, and potential stress-promoting functions. It is of great significance to explore the structure and salinity response of microbial communities in salt-tolerant plants to understand the mechanisms of plant-microbe interactions. Herein, we investigated the phyllosphere and rhizosphere microbial communities of Avicennia marina, a pioneer salt-tolerant plant, at three sites with different salinities in the coastal intertidal zone. The results showed that salinity had different effects on phyllosphere and rhizosphere microbial communities and had a greater impact on bacterial communities and bacterial network interactions. The rhizosphere bacterial community alpha diversity significantly increased with increasing salinity. Moreover, the relative abundance of Proteobacteria decreased significantly, while that of Bacteroidota and Actinobacteriota, with stronger salt tolerance and nutrient utilization capacity, increased significantly. Functional prediction indicated that the microbial communities could produce catalase, peroxidase, 3-phytase, and tryptophan synthase, which may exert potential antistress and growth-promoting functions. Among them, catalase, 3-phytase, alkaline phosphatase, and acid phosphatase increased significantly in the phyllosphere and rhizosphere bacterial communities and the phyllosphere fungal community with increasing salinity. Importantly, the dominant taxa Kushneria and Bacillus, which are salt tolerant and growth promoting, were isolated from the phyllosphere and rhizosphere, respectively, and verified to have the ability to alleviate salt stress and promote the growth of rice.IMPORTANCE Avicennia marina is a pioneer salt-tolerant plant in coastal intertidal mangroves, an efficient blue carbon ecosystem. It is of great importance to explore how salinity affects the phyllosphere and rhizosphere microbial communities of A. marina. This study showed that the microbial communities in the phyllosphere and rhizosphere of A. marina had different constitutive properties, adaptive network interactions, and potential stress-promoting functions. Furthermore, the dominant bacteria Kushneria and Bacillus were obtained from the phyllosphere and rhizosphere, respectively, and their coculture with rice could effectively alleviate salt stress and promote rice growth. Additionally, the effects of salinity changes on microbial community structure, associations, and functional potential in the phyllosphere and rhizosphere of A. marina were observed. This study has enriched our understanding of the microbial community structure, function, and ecological stability of mangrove species in coastal intertidal zones and has practical significance for improving crop yield by using salt-tolerant plant microbiomes.