Evolution and metabolic significance of the urea cycle in photosynthetic diatoms
Allen, A.E.; Dupont, C.L.; Obornik, M.; Horák, A.; Nunes-Nesi, A.; McCrow, J.P.; Zheng, H.; Johnson, D.A; Hu, H.; Fernie, A.R.; Bowler, C. (2011). Evolution and metabolic significance of the urea cycle in photosynthetic diatoms. Nature (Lond.) 473(7346): 203-207. https://dx.doi.org/10.1038/nature10074
In: Nature: International Weekly Journal of Science. Nature Publishing Group: London. ISSN 0028-0836; e-ISSN 1476-4687, more
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Keywords |
Algae > Diatoms Biological phenomena > Evolution Biology > Genetics Genomes Marine/Coastal |
Authors | | Top |
- Allen, A.E.
- Dupont, C.L.
- Obornik, M.
- Horák, A.
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- Nunes-Nesi, A.
- McCrow, J.P.
- Zheng, H.
- Johnson, D.A
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- Hu, H.
- Fernie, A.R.
- Bowler, C.
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Abstract |
Diatoms dominate the biomass of phytoplankton in nutrient-rich conditions and form the basis of some of the world's most productive marine food webs(1-4). The diatom nuclear genome contains genes with bacterial and plastid origins as well as genes of the secondary endosymbiotic host (the exosymbiont(5))(1,6-10), yet little is known about the relative contribution of each gene group to diatom metabolism. Here we show that the exosymbiont-derived ornithine-urea cycle, which is similar to that of metazoans but is absent in green algae and plants, facilitates rapid recovery from prolonged nitrogen limitation. RNA-interference-mediated knockdown of a mitochondrial carbamoyl phosphate synthase impairs the response of nitrogen-limited diatoms to nitrogen addition. Metabolomic analyses indicate that intermediates in the ornithine-urea cycle are particularly depleted and that both the tricarboxylic acid cycle and the glutamine synthetase/glutamate synthase cycles are linked directly with the ornithine-urea cycle. Several other depleted metabolites are generated from ornithine-urea cycle intermediates by the products of genes laterally acquired from bacteria. This metabolic coupling of bacterial-and exosymbiont-derived proteins seems to be fundamental to diatom physiology because the compounds affected include the major diatom osmolyte proline(12) and the precursors for long-chain polyamines required for silica precipitation during cell wall formation(11). So far, the ornithine-urea cycle is only known for its essential role in the removal of fixed nitrogen in metazoans. In diatoms, this cycle serves as a distribution and repackaging hub for inorganic carbon and nitrogen and contributes significantly to the metabolic response of diatoms to episodic nitrogen availability. The diatom ornithine-urea cycle therefore represents a key pathway for anaplerotic carbon fixation into nitrogenous compounds that are essential for diatom growth and for the contribution of diatoms to marine productivity. |
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