Co‐catabolism of arginine and succinate drives symbiotic nitrogen fixation

• Published in: Molecular systems biology 2020-06, Vol.16 (6), p.e9419-n/a
• Main Authors: Flores‐Tinoco, Carlos Eduardo, Tschan, Flavia, Fuhrer, Tobias, Margot, Céline, Sauer, Uwe, Christen, Matthias, Christen, Beat
• Format: Article
• Language: English
• Subjects: Adenosine Triphosphate - biosynthesis; Adenosine Triphosphate - metabolism; Agricultural engineering; Amination; Amino acids; Ammonium; Arginase - metabolism; Arginine; Arginine - metabolism; Bacteria; BASIC BIOLOGICAL SCIENCES; biological nitrogen fixation; Bradyrhizobium - genetics; Bradyrhizobium - physiology; Bradyrhizobium diazoefficiens; Carbon Isotopes; Catabolism; CATCH‐N cycle; Climate change; Dehydrogenases; DNA Transposable Elements - genetics; Electron Transport; EMBO21; EMBO23; EMBO30; Enzymes; Gene Deletion; Isotope Labeling; Legumes; Medicago - microbiology; Metabolic pathways; Metabolism; Nitrogen; Nitrogen Fixation; Nitrogenase - metabolism; Nitrogenation; Phenotype; Reducing agents; Sinorhizobium - genetics; Sinorhizobium - physiology; Sinorhizobium meliloti; Succinic Acid - metabolism; Sustainability; Sustainable agriculture; Symbiosis; Symbiosis - genetics; TnSeq; Transaminases
• ISSN: 1744-4292; 1744-4292
• DOI: 10.15252/msb.20199419

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 N 2 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. Synopsis This study challenges the current model of nitrogen exchange in rhizobia‐legumes symbiosis and describes the CATCH‐N cycle, which operates on the provision of arginine and succinate by the plant as part of a metabolic network driving symbiotic nitrogen fixation in rhizobia. The CATCH‐N cycle co‐catabolises plant‐provided arginine and succinate to drive the energy‐demanding process of symbiotic nitrogen fixation in endosymbiotic rhizobia. The CATCH‐N cycle functions as an effective mechanism to promote the survival of bacteroids within infected plant cells and results in a net gain of assimilated nitrogen that subsequently amplifies the plant's arginine biosynthesis capacity. The study represents an important step towards the rational engineering of artificial nitrogen‐fixing microbes. Graphical Abstract This study challenges the current model of nitrogen exchange in rhizobia‐legumes symbiosis and describes the CATCH‐