Microbial Diversity and Genome Analyses Provide Insights into the Role of Pseudomonas marginalis A39 in Improving Drought Tolerance in Pinus sylvestris var. mongolica

Drought severely constrains the growth of Pinus sylvestris var. mongolica, but the role of plant growth-promoting rhizobacteria in forest drought responses remains insufficiently understood. This study evaluated whether Pseudomonas marginalis A39 alleviates drought stress through plant physiological regulation, soil functional improvement, and rhizosphere bacterial community shifts. Strain A39 was first assessed for drought tolerance and plant growth-promoting traits in vitro. A greenhouse pot experiment was then conducted under graded drought levels with or without A39 inoculation, followed by analyses of plant growth, physiological traits, soil nutrients, enzyme activities, rhizosphere bacterial communities, whole-genome features, and drought-responsive gene expression. A39 tolerated low water potential and showed multiple growth-promoting traits. Under severe drought, A39 inoculation increased seedling height, ground diameter, aboveground dry weight, and underground dry weight by 83.58%, 47.69%, 37.14%, and 41.67%, respectively. It also increased total chlorophyll content and CAT activity by 30.38% and 40.20%, while reducing MDA and proline accumulation by 33.71% and 35.40%, respectively. A39 improved soil nutrient availability, with available nutrients increasing by more than 35%, and altered rhizosphere bacterial communities, with enrichment of taxa such as Pseudarthrobacter and Pseudomonas. Soil sucrase, available potassium, and total potassium were key factors associated with bacterial community variation. Genome annotation and qRT-PCR analysis identified candidate genes potentially related to nutrient acquisition, phytohormone production, oxidative stress defense, and osmotic adaptation. These results indicate that A39 inoculation is associated with improved drought performance of P. sylvestris var. mongolica, supporting its further evaluation as a candidate microbial inoculant for forest drought management.