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Co-catabolism of arginine and succinate drives symbiotic nitrogen fixation

View ORCID ProfileCarlos Eduardo Flores-Tinoco, View ORCID ProfileMatthias Christen, View ORCID ProfileBeat Christen
doi: https://doi.org/10.1101/741314
Carlos Eduardo Flores-Tinoco
aInstitute of Molecular Systems Biology, Eidgenössische Technische Hochschule (ETH) Zürich, CH-8093 Zürich, Switzerland
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  • ORCID record for Carlos Eduardo Flores-Tinoco
Matthias Christen
aInstitute of Molecular Systems Biology, Eidgenössische Technische Hochschule (ETH) Zürich, CH-8093 Zürich, Switzerland
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  • For correspondence: matthias.christen@imsb.biol.ethz.ch beat.christen@imsb.biol.ethz.ch
Beat Christen
aInstitute of Molecular Systems Biology, Eidgenössische Technische Hochschule (ETH) Zürich, CH-8093 Zürich, Switzerland
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  • For correspondence: matthias.christen@imsb.biol.ethz.ch beat.christen@imsb.biol.ethz.ch
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Abstract

Biological nitrogen fixation emerging from the symbiosis between bacteria and crop plants holds a significant promise to increase the sustainability of agriculture. One of the biggest hurdles for the engineering of nitrogen-fixing organisms is to identify the metabolic blueprint for symbiotic nitrogen fixation. Here, we report on the CATCH-N cycle, a novel metabolic network based on co-catabolism of 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 shares aspects with plant mitochondrial arginine degradation path-way. However, it 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 specific mechanism to sustain bacterial metabolism in the microoxic and acid environment of symbiosomes. In sum, our systems-level findings provide the theoretical framework and enzymatic blueprint for the rational design of plants and plant-associated organisms with new properties for improved nitrogen fixation.

Significance Statement Symbiotic bacteria assimilate nitrogen from the air and fix it into a form that can be used by plants in a process known as biological nitrogen fixation. In agricultural systems, this process is restricted mainly to legumes, yet there is considerable interest in exploring whether similar symbioses can be developed in non-legumes including cereals and other important crop plants. Here we present systems-level findings on the minimal metabolic function set for biological nitrogen fixation that provides the theoretical framework for rational engineering of novel organisms with improved nitrogen-fixing capabilities.

Footnotes

  • B.C. and CE.FT. performed transposon mutagenesis experiments; CE.FT. performed plant infection, nitrogenase and enzyme activity assays. M.C., B.C. and CE.FT. performed data analysis. M.C. and B.C. conceived the theoretical concept of the CATCH-N cycle; M.C. and B.C. wrote the manuscript.

  • The authors declare the following competing interests: B.C and M.C hold shares from Gigabases Switzerland AG.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted September 30, 2019.
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Co-catabolism of arginine and succinate drives symbiotic nitrogen fixation
Carlos Eduardo Flores-Tinoco, Matthias Christen, Beat Christen
bioRxiv 741314; doi: https://doi.org/10.1101/741314
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Co-catabolism of arginine and succinate drives symbiotic nitrogen fixation
Carlos Eduardo Flores-Tinoco, Matthias Christen, Beat Christen
bioRxiv 741314; doi: https://doi.org/10.1101/741314

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