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Plant growth-promoting rhizobacteria (PGPR) inoculation is a crucial strategy for maintaining the sustainability of agriculture and presents a promising solution for seagrass ecological restoration in the face of disturbances. However, the possible roles and functions of PGPRs in the seagrass rhizosphere remain unclear. Here, we isolated rhizosphere bacterial strains from both reef and coastal regions and screened two PGPR isolates regarding their in vivo functional traits. Subsequently, we conducted microcosm experiments to elucidate how PGPR inoculation affected seagrass photosynthesis and shape within each rhizosphere microbiome. Both screened PGPR strains, Raoultella terrigena NXT28 and Bacillus aryabhattai XT37, excelled at expressing a specific subset of plant-beneficial functions and increased the photosynthetic rates of the seagrass host. PGPR inoculation not only decreased the abundance of sulfur-cycling bacteria, it also improved the abundance of putative iron-cycling bacteria in the seagrass rhizosphere. Strain XT37 successfully colonized the seagrass rhizosphere and displayed a leading role in microbial network structure. As a nitrogen-fixing bacteria, NXT28 showed potential to change the microbial nitrogen cycle with denitrification in the rhizosphere and alter dissimilatory and assimilatory nitrate reduction in bulk sediment. These findings have implications for the development of eco-friendly strategies aimed at exploiting microbial communities to confer sulfide tolerance in coastal seagrass ecosystem. • Two PGPR strains were screened from different seagrass species in both reef and coastal regions. • PGPR strains increased the photosynthetic rates of seagrass host. • PGPR inoculation inhibited and enriched the abundance of iron- and sulfur-cycling bacterial taxa, respectively. • The colonization of the seagrass rhizosphere by Bacillus aryabhattai XT37 played a leading role in the microbial network. [ABSTRACT FROM AUTHOR]