Gu Yian, Yan Wenhui, Chen Yu, Liu Sijie, Sun Liang, Zhang Zhe, Lei Peng, Wang Rui, Li Sha, Banerjee Samiran, Friman Ville-Petri, Xu Hong
State Key Laboratory of Materials-Oriented Chemical Engineering, Nanjing Tech University, No. 30 Puzhu South Road, Jiangbei New District, Nanjing 211816, PR China.
Key Laboratory of Water-saving Agriculture of Northeast, Ministry of Agriculture and Rural Affairs, Liaoning Academy of Agricultural Science, No. 84 Dongling Road, Shenhe District, Shenyang 110161, PR China.
ISME J. 2025 Jan 2;19(1). doi: 10.1093/ismejo/wraf040.
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.
尽管根际微生物群在植物生长中发挥着关键作用，但通过操纵微生物群落来提高植物生产力仍然具有挑战性。原因之一是缺乏关于微生物群中分泌的复杂底物如何最终影响与植物生长相关的微生物-微生物以及植物-微生物相互作用的知识。聚-γ-谷氨酸就是这样一种复杂底物，它是一种微生物来源的细胞外聚合物。虽然此前已将其与植物生长促进联系起来，但其潜在机制尚未得到充分理解。在这里，我们表明这种化合物通过促进根际细菌之间的交叉喂养网络使植物受益。我们首先通过实验证明，施用聚-γ-谷氨酸可通过驱动根际细菌群落组成的变化来提高番茄植株对钾的生物有效性。具体而言，施用聚-γ-谷氨酸增加了硝基还原假单胞菌L16和蒙氏假单胞菌L20的相对丰度，这两种细菌分别通过分泌溶解钾的丙酮酸和螯合钾的铁载体来促进番茄对钾的吸收。尽管任何一种假单胞菌菌株都不能直接代谢聚-γ-谷氨酸，但施用聚-γ-谷氨酸促进了芽孢杆菌属细菌的生长，而芽孢杆菌属细菌又产生了可促进硝基还原假单胞菌L16和蒙氏假单胞菌L20生长的代谢产物。此外，蒙氏假单胞菌L20产生的3-羟基癸酸可促进硝基还原假单胞菌L16的生长，从而在促进植物生长的细菌之间形成共生交叉喂养相互作用。总之，这些结果表明聚-γ-谷氨酸在通过细菌交叉喂养网络促进植物生长方面发挥着关键作用，突出了利用微生物来源的复杂底物作为催化剂来提高农业生产力的机会。
