A Synergistic Indole-3-Acetic Acid-Producing Synthetic Bacterial Consortium Benefits Walnut Seedling Growth

Synthetic microbial communities (SynComs) have been shown to be an ecofriendly alternative for promoting plant growth. However, the mechanisms by which SynCom inoculants drive plant growth promotion in rhizosphere soil are still not fully explored. Herein, we designed a three-strain consortium based on the biocompatibility among strains and indole-3-acetic acid (IAA) production. The consortium containing Bacillus safensis 5-49, Bacillus stratosphericus 5-54, and Bacillus halotolerans 6-30 possessed a synergistic effect on IAA production and biofilm formation. Genetic analysis suggested that IAA was synthesized through tryptophan-dependent pathways in the strains. The consortium outperformed the plant growth-promoting effect observed with single strains, showing an increase in walnut (Juglans regia) seedling dry weight by 92.3% over the non-inoculated plants after 60 days of cultivation. This effect was underpinned by the synergistic interactions of the consortium, which was evidenced by the significantly increased relative abundance of Bacillus and tryptophan metabolism-associated genes in the rhizosphere of consortium-inoculated plants. Meanwhile, the consortium increased the relative abundance of indigenous Pseudomonas in rhizosphere soil, providing a synergistic effect on improving soil enzyme activities and thus available nutrients. The available N, P, and K contents in the consortium-inoculated plant rhizosphere were 3.77–28.4% higher than those in non-inoculated samples. This work provided an efficient bacterial consortium and proposed the mode of action by which this consortium improved plant growth and soil fertility.