Plant growth-promotion triggered by extracellular polymer is associated with facilitation of bacterial cross-feeding networks of the rhizosphere

Despite the critical role rhizosphere microbiomes play in plant growth, manipulating microbial communities for improved plant productivity remains challenging. One reason for this is the lack of knowledge on how complex substrates secreted in the microbiome ultimately shape the microbe-microbe and plant-microbe interaction in relation to plant growth. One such complex substrate is poly-γ-glutamic acid, which is a microbially derived extracellular polymer. While it has previously been linked with plant growth-promotion, the underlying mechanisms are not well understood. Here, we show that this compound benefits plants by fostering cross-feeding networks between rhizosphere bacteria. We first experimentally demonstrate that poly-γ-glutamic acid application increases potassium bioavailability for tomato plants by driving a shift in the rhizosphere bacterial community composition. Specifically, application of poly-γ-glutamic acid increased the relative abundance of Pseudomonas nitroreducens L16 and Pseudomonas monteilii L20 bacteria which both promoted tomato potassium assimilation by secreting potassium-solubilizing pyruvic acid and potassium-chelating siderophores, respectively. Although either Pseudomonas strain could not metabolize poly-γ-glutamic acid directly, the application of poly-γ-glutamic acid promoted the growth of Bacillus species, which in turn produced metabolites that could promote the growth of both P. nitroreducens L16 and P. monteilii L20. Moreover, the P. monteilii L20 produced 3-hydroxycapric acid, which could promote the growth of P. nitroreducens L16, resulting in commensal cross-feeding interaction between plant growth-promoting bacteria. Together, these results show that poly-γ-glutamic acid plays a crucial role in driving plant growth-promotion via bacterial cross-feeding networks, highlighting the opportunity for using microbially derived, complex substrates as catalysts to increase agricultural productivity.