Plant growth depends on a range of functions provided by their associated rhizosphere microbiome, including nutrient mineralization, hormone co-regulation and pathogen suppression. Improving the ability of plant-associated microbiomes to deliver these functions is thus important for developing robust and sustainable crop production. However, it is yet unclear how beneficial effects of probiotic microbial inoculants can be optimized and how their effects are mediated. Here, we sought to enhance tomato plant growth by targeted introduction of probiotic bacterial consortia consisting of up to eight plant-associated Pseudomonas strains. We found that the effect of probiotic consortium inoculation was richness-dependent: consortia that contained more Pseudomonas strains reached higher densities in the tomato rhizosphere and had clearer beneficial effects on multiple plant growth characteristics. Crucially, these effects were best explained by changes in the resident community diversity, composition and increase in the relative abundance of initially rare taxa, instead of introduction of plant-beneficial traits into the existing community along with probiotic consortia. Together, our results suggest that beneficial effects of microbial introductions can be driven indirectly through effects on the diversity and composition of the resident plant rhizosphere microbiome.

Bio-organic fertilization is a widely used, eco-friendly, sustainable approach to increasing plant productivity in the agriculture and fruit industries. However, it remains unclear whether the promotion of fruit productivity is related to specific changes in microbial inoculants, the resident microbiome, and/or the physicochemical properties of rhizosphere soils.

The soil-borne bacterial pathogen Ralstonia solanacearum causes significant losses in Solanaceae crop production worldwide, including tomato, potato, and eggplant. To efficiently prevent outbreaks, it is essential to understand the complex interactions between pathogens and the microbiome. One promising mechanism for enhancing microbiome functionality is siderophore-mediated competition, which is shaped by the low iron availability in the rhizosphere. This study explores the critical role of iron competition in determining microbiome functionality and its potential for designing high-performance microbiome engineering strategies. We investigated the impact of siderophore-mediated interactions on the efficacy of Pseudomonas spp. consortia in suppressing R. solanacearum, both in vitro and in vivo. Our findings show that siderophore production significantly enhances the inhibitory effects of Pseudomonas strains on pathogen growth, while other metabolites are less effective under iron-limited conditions. Moreover, siderophores play a crucial role in shaping interactions within the consortia, ultimately determining the level of protection against bacterial wilt disease. This study highlights the key role of siderophores in mediating consortium interactions and their impact on tomato health. Our results also emphasize the limited efficacy of other secondary metabolites in iron-limited environments, underscoring the importance of siderophore-mediated competition in maintaining tomato health and suppressing disease.

Iron bioavailability is often limited especially in calcareous soils. Trichoderma harzianum strongly improves plant iron uptake and growth in calcareous soils. However, little is known about the mechanisms by which T. harzianum mobilizes iron in calcareous soils. Here, the model strain T. harzianum NJAU4742 and a synthetic microbial community (SynCom) was used to show that the efficacy of T. harzianum in enhancing plant iron nutrition in calcareous soils depends on the soil microbiome. Enhanced iron-mobilization functions of the SynCom were observed in the presence of T. harzianum NJAU4742. Concurrently, T. harzianum NJAU4742 improved the iron-mobilization capacity of the SynCom by enriching strains that are able to do so. Finally, Chryseobacterium populi was identified as a key driver of iron mobilization, while their synergistic colonization further enhances this process. This study unveils a pivotal mechanism by which T. harzianum NJAU4742-mediated re-structuring of the soil microbiome and ameliorates plant iron nutrition.

Root exudates are key mediators in maintaining plant health by mediating interactions with the rhizosphere microbiome. Plants release specific exudates to defend against pathogens, either directly by inhibiting pathogen growth or indirectly through alterations in the microbial community. However, the mechanisms by which root exudates influence the rhizosphere microbiome to enhance plant resistance remain poorly understood. In this study, we evaluated the effects of 23 root exudates on the growth of the pathogen Ralstonia solanacearum and tomato bacterial wilt. Seventeen of the exudates reduced the disease index, with most having neutral or even promotive effects on R. solanacearum growth. Notably, succinic acid (SA) completely suppressed bacterial wilt without directly affecting the pathogen or tomato plants in the absence of the rhizosphere microbiome. We further explored the impact of SA on the rhizosphere bacterial community in both tomato rhizosphere and bulk soil. Only the bacterial community in the rhizosphere responded significantly to SA addition, with indicator species and network analyses identifying Sphingomonas sp. WX113 as the key taxa associated with this response. A subsequent greenhouse experiment showed that co-applying Sphingomonas sp. WX113 with SA achieved 100% biocontrol efficiency, outperforming either treatment alone. In vitro assays further demonstrated that SA enhanced the antagonistic activity of Sphingomonas sp. WX113 against R. solanacearum. Our findings emphasize the host-mediated role of root exudates, such as succinic acid, in selectively promoting beneficial Sphingomonas sp., thereby enhancing plant resistance to bacterial wilt. These results offer new perspectives on the combination of beneficial microbes and their matching compounds for soil-borne diseases management.