Biological nitrogen fixation emerging from the symbiosis between bacteria and crop plants holds promise to increase the sustainability of agriculture. One of the biggest hurdles for the engineering of nitrogen‐fixing organisms is an incomplete knowledge of metabolic interactions between microbe and plant. In contrast to the previously assumed supply of only succinate, we describe here the CATCH ‐N cycle as a novel metabolic pathway that co‐catabolizes plant‐provided arginine and succinate to drive the energy‐demanding process of symbiotic nitrogen fixation in endosymbiotic rhizobia. Using systems biology, isotope labeling studies and transposon sequencing in conjunction with biochemical characterization, we uncovered highly redundant network components of the CATCH ‐N cycle including transaminases that interlink the co‐catabolism of arginine and succinate. The CATCH ‐N cycle uses N₂ as an additional sink for reductant and therefore delivers up to 25% higher yields of nitrogen than classical arginine catabolism—two alanines and three ammonium ions are secreted for each input of arginine and succinate. We argue that the CATCH ‐N cycle has evolved as part of a synergistic interaction to sustain bacterial metabolism in the microoxic and highly acid environment of symbiosomes. Thus, the CATCH ‐N cycle entangles the metabolism of both partners to promote symbiosis. Our results provide a theoretical framework and metabolic blueprint for the rational design of plants and plant‐associated organisms with new properties to improve nitrogen fixation.

中文翻译：

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精氨酸和琥珀酸酯的共分解代谢驱动共生固氮。

细菌与农作物之间共生的生物固氮技术有望提高农业的可持续性。固氮生物工程的最大障碍之一是对微生物与植物之间代谢相互作用的不完全了解。与以前假定的仅琥珀酸的供应量相反，我们在这里将CATCH ‐N循环描述为一种新的代谢途径，该途径共分解代谢植物提供的精氨酸和琥珀酸，从而驱动内共生根瘤菌中共生固氮的能量需求过程。利用系统生物学，同位素标记研究和转座子测序结合生化表征，我们发现了CATCH ‐N循环中高度冗余的网络组件，包括使精氨酸和琥珀酸酯的共分解代谢相互联系的转氨酶。CATCH-N循环使用N₂作为还原剂的附加吸收剂，因此比传统的精氨酸分解代谢提供高25％的氮产率-精氨酸和琥珀酸的每次输入都会分泌两个丙氨酸和三个铵离子。我们认为，CATCH-N循环是协同相互作用的一部分，可在共生体的微氧和高酸环境中维持细菌代谢。因此，CATCH-N循环纠缠了双方的新陈代谢，从而促进了共生。我们的结果为合理设计具有新特性以改善固氮作用的植物和植物相关生物提供了理论框架和代谢蓝图。