Co‐catabolism of arginine and succinate drives symbiotic nitrogen fixation
Open Access
- 3 June 2020
- journal article
- research article
- Published by Springer Science and Business Media LLC in Molecular Systems Biology
- Vol. 16 (6)
- https://doi.org/10.15252/msb.20199419
Abstract
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.Keywords
Funding Information
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (31003A_166476, 310030_184664, CRSII5_177164)
This publication has 77 references indexed in Scilit:
- Adaptation of maize source leaf metabolism to stress related disturbances in carbon, nitrogen and phosphorus balanceBMC Genomics, 2013
- Refactoring the nitrogen fixation gene cluster fromKlebsiella oxytocaProceedings of the National Academy of Sciences of the United States of America, 2012
- The essential genome of a bacteriumMolecular Systems Biology, 2011
- The lss Supernodulation Mutant of Medicago truncatula Reduces Expression of the SUNN GenePlant Physiology, 2010
- Fast and accurate long-read alignment with Burrows–Wheeler transformBioinformatics, 2010
- Tn-seq: high-throughput parallel sequencing for fitness and genetic interaction studies in microorganismsNature Methods, 2009
- Climbing Nitrogenase: Toward a Mechanism of Enzymatic Nitrogen FixationAccounts of Chemical Research, 2009
- Characterization of an Arginine:Pyruvate Transaminase in Arginine Catabolism of Pseudomonas aeruginosa PAO1Journal of Bacteriology, 2007
- Functional Genomics Enables Identification of Genes of the Arginine Transaminase Pathway in Pseudomonas aeruginosaJournal of Bacteriology, 2007
- Global protein expression pattern ofBradyrhizobium japonicum bacteroids: A prelude to functional proteomicsProteomics, 2005