Abstract: Aims Phyllosphere microorganisms are pivotal in mediating plant nutrient cycling and promoting host stress tolerance. Yet, for mangrove plants distributed along tidal gradients, the response patterns and driving mechanisms of phyllosphere microbiomes to intertidal environmental gradients remain to be deeply investigated. Methods This study focused on two mangrove species, Aegiceras corniculatum and Avicennia marina, occurring across low (LT), middle (MT), and high (HT) tidal elevations in the Dongzhai Harbor National Nature Reserve, Hainan, China. We compared the community characteristics of epiphytic and endophytic bacterial and fungal assemblages in the phyllosphere across different tidal elevations, parsed the explanatory power of host identity and tidal gradients on community structural differences, and quantified the relative contributions of environmental factors versus leaf physicochemical traits to community structure. Important findings With the exception of endophytic fungi, which exhibited the highest number of unique amplicon sequence variants (ASVs) at HT, the other three phyllosphere communities harbored the greatest numbers of unique ASVs at LT. Richness and diversity of both bacterial and fungal communities differed significantly among tidal elevations. Community composition was dominated by the bacterial phyla Pseudomonadota, Actinomycetota, and Bacteroidota, and by the fungal phyla Ascomycota and Basidiomycota. Driving mechanism analysis revealed that host identity was the primary driver of bacterial community differentiation, whereas fungal community structure was significantly shaped by the interaction between host identity and tidal elevation. Correlation analyses further indicated that leaf functional traits—particularly total calcium and total potassium—explained a significantly larger unique fraction of community variation than did environmental factors such as salinity and temperature. Furthermore, dominant genera exhibited significant associations with specific environmental variables and leaf functional traits. Collectively, these results suggest that mangrove phyllosphere microbiome assembly arises from joint effects of host traits and tidal environments: host-specific physicochemical traits determine the baseline characteristics of the community, while the tidal gradient exerts secondary regulation on community diversity through environmental filtering. These findings clarify the phyllosphere microbial adaptation strategies of different mangrove plants in response to tidal habitat heterogeneity and deepen our understanding of the “host–environment–microbe” interaction mechanisms in mangrove phyllosphere microecosystems.

Key words: Phyllosphere, Mangrove, Tidal elevations, Community characteristics, Leaf functional traits