Adaptive responses of different halophytes to soil water stress regulate the composition, diversity, and functional differentiation of their phyllosphere microbial communities

Background: In saline ecosystems, halophytes reshape their phyllosphere microenvironment through unique salt-tolerance strategies, driving microbial community differentiation and functional adaptation. But under extreme conditions, a comprehensive understanding of how these microbes respond to environmental cues and subsequently influence their hosts remains elusive. Methods: Leaf physiological-biochemical traits and high-throughput amplicon sequencing data of phyllosphere microbiota from three representative halophytes—Suaeda salsa (SS), Nitraria sibirica (NS), and Salicornia europaea (SE)—were collected and analyzed along gradients of soil salinity and water content. Results: Soil water stress, induced by the combined effects of soil salinity and moisture, is a pivotal factor driving differences in plant physiological-biochemical traits. Under the influence of these trait variations, deterministic processes jointly governed the assembly of phyllosphere bacterial and fungal communities, yet their composition, diversity, and metabolic functions exhibited marked differences. Specifically, the key bacterial genus Planococcus, fungal taxa within Ascomycota, and metabolic functions associated with antioxidant stress responses were significantly enhanced in SS; the bacterial genus Vibrio and metabolic functions linked to microbial competition-defense mechanisms and oligotrophic traits were enhanced in SE. Varying degrees of increase in key fungal and bacterial taxa across the phyllosphere of all three species further influenced community diversity, but stochastic processes also contributed to fungal community assembly. Conclusions: Findings reveal that soil water stress indirectly impacts phyllosphere microbial communities, with differences in the stress-tolerant physiological-biochemical traits of halophytes under varying water stress conditions significantly shaping microbial community composition. Moreover, the stress-resistance traits exhibited by phyllosphere microbiota may enhance plant adaptation to extreme environments.