Temporal dynamics of the tomato rhizosphere microbiome in response to synthetic communities of plant growth-promoting rhizobacteria

The rhizosphere microbiome plays a crucial role in plant health and productivity, yet intensive agriculture has diminished soil microbial diversity, increasing reliance on chemical inputs. Plant growth-promoting rhizobacteria offer a sustainable alternative, enhancing nutrient uptake, stress tolerance, and pathogen resistance. While single-strain inoculants have shown promise, microbial consortia may improve resilience through functional diversity. However, their impact on resident microbial communities remains understudied. In this study, three SynComs (four, six, and ten strains) were assembled from taxonomically diverse native PGPR strains identified as part of the tomato core microbiome, including Bacillus, Pseudomonas, Glutamicibacter, Paenarthrobacter, Chryseobacterium and Leclercia. All consortia significantly enhanced tomato growth, with the six- and ten-strain SynComs (containing Pseudomonas) exhibiting the most pronounced effects, increasing plant height by up to 94% in the indeterminate-growth variety ‘Proxy’. High-throughput sequencing revealed that while temporal factors were the primary drivers of community assembly, SynCom application triggered dynamic, time-dependent shifts specifically targeting the bacterial “rare biosphere”. Early-stage (T1) responses were characterized by the enrichment of rare bacterial taxa involved in key biogeochemical processes, such as the sulphur (Sulfurovum, Desulfosporosinus) and nitrogen (Azospirillum) cycles. By four weeks post-inoculation, community responses converged, primarily through the depletion of rare taxa and a predicted functional redirection toward xenobiotic degradation pathways. While SynCom strains showed a decline in absolute abundance over time, the persistence of growth-promoting effects suggests that these consortia act through early-stage indirect microbiome modulation rather than long-term high-density colonization. Furthermore, the consortia exerted a subtle cross-kingdom influence, modulating fungal succession by sustaining Basidiomycota and Mucoromycota populations. These findings demonstrate that small, host-derived, taxonomically diverse SynComs can enhance tomato growth and restructure rhizosphere microbial communities, especially impacting rare bacterial taxa and metabolic potential of the communities, with Pseudomonas-containing consortia exerting the most pronounced effects. These insights support the use of tailored, core-based microbial communities to improve crop productivity and soil health, though further research is needed to optimize SynCom design for agricultural applications.