Insights into Genomic Evolution and the Potential Genetic Basis of Klebsiella variicola subsp. variicola ZH07 Reveal Its Potential for Plant Growth Promotion and Autotoxin Degradation

The accumulation of autotoxins in soil causes continuous cropping obstacle stress in crops, and the bioremediation of autotoxins by microorganisms is an efficient process. In this study, strain ZH07 was isolated from the peanut rhizosphere and was found to be utilizing multiple autotoxins as its carbon sources. Based on its genomic characteristics and a phylogenetic analysis, ZH07 represents a member of Klebsiella variicola subsp. variicola. A comparative genomic analysis exhibited evolutionary dynamics exhibited by mobile genetic elements (MGEs), strain-specific genes, potential horizontal genes, and evolutionary constraints driven by purifying selection, which facilitated its genomic adaptation to rhizosphere soil. Genome mining revealed the potential genomic properties associated with plant growth promotion, such as nitrogen fixation, indole acetic acid synthesis, phosphonate solubilization and assimilation, siderophore production, and secondary metabolite synthesis. Moreover, abundant genes putatively responsible for the biodegradation of aromatic xenobiotics, including benzoic acid, cinnamic acid, vanillic acid, protocatechuic acid, phenylacetic acid, and p-hydroxybenzoic acid were also observed in the ZH07 genome. Compared to autotoxin stress alone, the combination of ZH07 application promoted peanut germination and seedling growth. Our analysis revealed the genetic adaptation of ZH07 to the rhizosphere environment and the potential genetic basis and effectiveness of the isolate to serve as a plant growth stimulator. IMPORTANCE Continuous cropping obstacles reduce the production and quality of agricultural products, and the application of rhizosphere beneficial microbes is an important strategy. Strain ZH07 showed autotoxin-degrading and plant growth-promoting capacities. The objectives of this study were to characterize its genomic evolution and the potential genetic basis of the autotoxin degradation and plant growth promotion. ZH07 represents a member of Klebsiella variicola subsp. variicola, based on genomic and phylogenetic analyses. Its genomic components have undergone different degrees of purifying selection, and the disparity in the evolutionary rate may be associated with its niche adaptation. A systematic analysis of the ZH07 genome identified the potential genetic basis that contributes to plant growth promotion and to aromatic xenobiotic biodegradation. This study demonstrates that plant growth-promoting rhizobacteria (PGPR) play important roles in autotoxin biodegradation and can be used as biofertilizers to enhance the growth of peanuts in response to continuous cropping obstacle stress.