Abstract
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.
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Acknowledgements
This work was financially supported by the National Nature Science Foundation of China (31972512, 32072675, and 32072665), the Agricultural Science and Technology Innovation Program of CAAS (CAAS-ZDRW202009), the Fundamental Research Funds for the Central Universities (KYXK202009). XS was supported by a Chinese Scholarship Council fellowship. ÁTK, MLS, and AD were supported by the Danish National Research Foundation (DNRF137) for the Center for Microbial Secondary Metabolites. AD was supported by Slovenian Research Agency (N1-0177). Biofilm-related work in the group of ÁTK is supported by a DTU Alliance Strategic Partnership PhD fellowship. Funding from Novo Nordisk Foundation (grant NNFOC0055625) for the infrastructure “Imaging microbial language in biocontrol (IMLiB)” is acknowledged. Author XS is very grateful to Prof. Shen and Prof. Zhang for the strong supports during the period of outbreak epidemics of COVID-19.
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XS, ZX, RZ, and ÁTK designed the study; XS, JX, and TT performed the experiments. XS, VHT, and MLS analyzed the data and created the figures. DZ constructed the metabolic models. XS and ZX wrote the first draft of the paper; AD, ÁTK, MLS, RZ, and QS revised the paper.
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Sun, X., Xu, Z., Xie, J. et al. Bacillus velezensis stimulates resident rhizosphere Pseudomonas stutzeri for plant health through metabolic interactions. ISME J 16, 774–787 (2022). https://doi.org/10.1038/s41396-021-01125-3
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DOI: https://doi.org/10.1038/s41396-021-01125-3
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