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The bacteria that dominate and become enriched in the rhizosphere during continuous cropping are of increasing interest, as they can greatly adapt to the rhizosphere. However, there are still little knowledge about the general composition and function of these bacteria. In this study, we planted tomatoes in three different soils for three planting cycles and used both high-throughput sequencing and culture-dependent workflows. Despite significant differences in bacterial communities from the initial soils, we observed a similar succession in the rhizosphere bacterial community compositions. We identified certain bacteria that were gradually enriched and potentially beneficial, such as Rhizobium and Flavobacterium. However, some other potentially beneficial bacteria, such as Massilia and Lysobacter, were gradually depleted. Additionally, we found that predicted functions related to xenobiotic biodegradation, nutrient metabolism and antibiotic biosynthesis were enriched in different rhizosphere soils. Beijerinckia fluminensis GR2, which was gradually enriched in all tested soils, significantly inhibited the growth of Ralstonia solanacearum and protected the host from infection. Our study provides new insights into the assembly mechanism of gradually enriched bacteria and their role as plant-beneficial microbes that adapt well to the rhizosphere.

Phenolic acids are mainly released from plant residue decomposition and play important roles in the assembly of the soil microbiome. Understanding the general features of soil microbial communities modulated by phenolic acids could provide fundamental insights into the assembly of the soil microbiome. We analyzed the effects of four phenolic acids (ferulic acid, phthalic acid, salicylic acid and tannic acid) on the soil fungal communities at two concentrations. Despite the application of different phenolic acids to the soil, we were able to identify certain general changes in the fungal communities. We found that the tested phenolic acids significantly increased the deterministic assembly process of the fungal community but decreased the fungal diversity. Moreover, the fungal community structure under each tested phenolic acid treatment was distinct at low concentrations but similar at high concentrations. Salicylic acid had the greatest impacts on the fungal community. In addition, Fusarium and Aspergillus were significantly enriched in the soil amended with all the tested phenolic acids at high concentrations. Our study revealed certain general changes in the soil fungal communities modulated by phenolic acids, which deepened our understanding of the fungal assembly mechanism and provided robust insights for identifying candidate phenolic acid-degrading microbes.

Competition for iron is an important factor for microbial niche establishment in the rhizosphere. Pathogenic and beneficial symbiotic bacteria use various secretion systems to interact with their hosts and acquire limited resources from the environment. Bacillus spp. are important plant commensals that encode a type VII secretion system (T7SS). However, the function of this secretion system in rhizobacteria–plant interactions is unclear. Here we use the beneficial rhizobacterium Bacillus velezensis SQR9 to show that the T7SS and the major secreted protein YukE are critical for root colonization. In planta experiments and liposome-based experiments demonstrate that secreted YukE inserts into the plant plasma membrane and causes root iron leakage in the early stage of inoculation. The increased availability of iron promotes root colonization by SQR9. Overall, our work reveals a previously undescribed role of the T7SS in a beneficial rhizobacterium to promote colonization and thus plant–microbe interactions.

ABSTRACT Microbes typically reside in communities containing multiple species, whose interactions have considerable impacts on the robustness and functionality of such communities. To manage microbial communities, it is essential to understand the factors driving their assemblage and maintenance. Even though the community composition could be easily assessed, interspecies interactions during community establishment remain poorly understood. Here, we combined co-occurrence network analysis with quantitative PCR to examine the importance of each species within synthetic communities (SynComs) of pellicle biofilms. Genome-scale metabolic models and in vitro experiments indicated that the biomass of SynComs was primarily affected by keystone species that are acting either as metabolic facilitators or as competitors. Our study sets an example of how to construct a SynCom and investigate interspecies interactions. IMPORTANCE Co-occurrence network analysis is an effective tool for predicting complex networks of microbial interactions in the natural environment. Using isolates from a rhizosphere, we constructed multi-species biofilm communities and investigated co-occurrence patterns between microbial species in genome-scale metabolic models and in vitro experiments. According to our results, metabolic exchanges and resource competition may partially explain the co-occurrence network analysis results found in synthetic bacterial biofilm communities.

Tropical and subtropical acidic soils are hotspots of global terrestrial nitrous oxide (N2O) emissions, with N2O produced primarily through denitrification. Plant growth-promoting microbes (PGPMs) may effectively mitigate soil N2O emissions from acidic soils, achieved through differential responses of bacterial and fungal denitrification to PGPMs. To test this hypothesis, we conducted a pot experiment and the associated laboratory trials to gain the underlying insights into the PGPM Bacillus velezensis strain SQR9 effects on N2O emissions from acidic soils. SQR9 inoculation significantly reduced soil N2O emissions by 22.6–33.5 %, dependent on inoculation dose, and increased the bacterial AOB, nirK and nosZ genes abundance, facilitating the reduction of N2O to N2 in denitrification. The relative contribution of fungi to the soil denitrification rate was 58.4–77.1 %, suggesting that the N2O emissions derived mainly from fungal denitrification. The SQR9 inoculation significantly inhibited the fungal denitrification and down-regulated fungal nirK gene transcript, dependent on the SQR9 sfp gene, which was necessary for secondary metabolite synthesis. Therefore, our study provides new evidence that decreased N2O emissions from acidic soils can be due to fungal denitrification inhibited by PGPM SQR9 inoculation., Tropical and subtropical acidic soils are hotspots of global terrestrial nitrous oxide (N2O) emissions, with N2O produced primarily through denitrification. Plant growth-promoting microbes (PGPMs) may effectively mitigate soil N2O emissions from acidic soils, achieved through differential responses of bacterial and fungal denitrification to PGPMs. To test this hypothesis, we conducted a pot experiment and the associated laboratory trials to gain the underlying insights into the PGPM Bacillus velezensis strain SQR9 effects on N2O emissions from acidic soils. SQR9 inoculation significantly reduced soil N2O emissions by 22.6–33.5 %, dependent on inoculation dose, and increased the bacterial AOB, nirK and nosZ genes abundance, facilitating the reduction of N2O to N2 in denitrification. The relative contribution of fungi to the soil denitrification rate was 58.4–77.1 %, suggesting that the N2O emissions derived mainly from fungal denitrification. The SQR9 inoculation significantly inhibited the fungal denitrification and down-regulated fungal nirK gene transcript, dependent on the SQR9 sfp gene, which was necessary for secondary metabolite synthesis. Therefore, our study provides new evidence that decreased N2O emissions from acidic soils can be due to fungal denitrification inhibited by PGPM SQR9 inoculation.

High-throughput sequencing, culture-dependent workflows, and microbiome transfer experiments reveal whether potassium phosphite (KP), an environmentally acceptable agricultural chemical, could specifically enrich the antagonistic bacterial community that inhibited the growth of the pathogen Ralstonia solanacearum. The application of KP enriched the potential antagonistic bacteria Paenibacillus and Streptomyces in soil, but depleted most dominant genera belonging to gram negative bacteria, such as Pseudomonas, Massilia, and Flavobacterium on day 7. Moreover, the KP-modulated soil microbiome suppressed R. solanacearum growth in soil. The predicted functions related to the synthesis of antagonistic substances, such as streptomycin, and the predicted functions related to tellurite resistance and nickel transport system were significantly enriched, but the synthesis of lipopolysaccharide (distinct component lipopolysaccharide in gram negative bacteria) were significantly depleted in the KP-treated soils. In addition, the copy numbers of specific sequences for Streptomyces coelicoflavus and Paenibacillus favisporus were significantly increased in the soil amended with KP, inhibited the growth of R. solanacearum, and had a higher tolerance of KP than R. solanacearum. Our study linked the application of fertilizers to the enrichment of antagonistic bacteria, which could support future work that aims to precisely regulate the soil microbiome to protect the host from infection by soil-borne pathogens.

Bacterial wilt caused by Ralstonia solanacearum is a distributed and worldwide soilborne disease. The application of biocontrol microbes or agricultural chemicals has been widely used to manage tomato bacterial wilt. However, whether and how agricultural chemicals affect the antagonistic ability of biocontrol microbes is still unknown. Here, we combined potassium phosphite (K-Phite), an environmentally friendly agricultural chemical, and the biocontrol agent Bacillus amyloliquefaciens QPF8 (strain F8) to manage tomato bacterial wilt disease. First, K-Phite at a concentration of 0.05% (wt/vol) could significantly inhibit the growth of R. solanacearum. Second, 0.05% K-Phite enhanced the antagonistic capability of B. amyloliquefaciens F8. Third, the greenhouse soil experiments showed that the control efficiency for tomato bacterial wilt in the combined treatment was significantly higher than that of the application of B. amyloliquefaciens F8 or K-Phite alone. Overall, our results highlighted a novel strategy for the control of tomato bacterial wilt disease via application and revealed a new integrated pattern depending on the enhancement of the antagonistic capability of biocontrol microbes by K-Phite.

Trophic interactions play a central role in driving microbial community assembly and function. In gut or soil ecosystems, successful inoculants are always facilitated by efficient colonization; however, the metabolite exchanges between inoculants and resident bacteria are rarely studied, particularly in the rhizosphere. Here, we used bioinformatic, genetic, transcriptomic, and metabonomic analyses to uncover syntrophic cooperation between inoculant (Bacillus velezensis SQR9) and plant-beneficial indigenous Pseudomonas stutzeri in the cucumber rhizosphere. We found that the synergistic interaction of these two species is highly environmental dependent, the emergence of syntrophic cooperation was only evident in a static nutrient-rich niche, such as pellicle biofilm in addition to the rhizosphere. Our results identified branched-chain amino acids (BCAAs) biosynthesis pathways are involved in syntrophic cooperation. Genome-scale metabolic modeling and metabolic profiling also demonstrated metabolic facilitation among the bacterial strains. In addition, biofilm matrix components from Bacillus were essential for the interaction. Importantly, the two-species consortium promoted plant growth and helped plants alleviate salt stress. In summary, we propose a mechanism in which synergic interactions between a biocontrol bacterium and a partner species promote plant health.