Common origin of ornithine\u2013urea cycle in opisthokonts and stramenopiles

Aleš Horák,Andrew E Allen,Miroslav Oborník

doi:10.1038/s41598-020-73715-8

Abstract

Eukaryotic complex phototrophs exhibit a colorful evolutionary history. At least three independent endosymbiotic events accompanied by the gene transfer from the endosymbiont to host assembled a complex genomic mosaic. Resulting patchwork may give rise to unique metabolic capabilities; on the other hand, it can also blur the reconstruction of phylogenetic relationships. The ornithine–urea cycle (OUC) belongs to the cornerstone of the metabolism of metazoans and, as found recently, also photosynthetic stramenopiles. We have analyzed the distribution and phylogenetic positions of genes encoding enzymes of the urea synthesis pathway in eukaryotes. We show here that metazoan and stramenopile OUC enzymes share common origins and that enzymes of the OUC found in primary algae (including plants) display different origins. The impact of this fact on the evolution of stramenopiles is discussed here.

Highlights

Eukaryotic complex phototrophs exhibit a colorful evolutionary history
We have shown recently that RNAi knockdown of carbamoylphosphate synthase (CPS), the key enzyme supplying the ornithine–urea cycle (OUC) pathway with carbon and nitrogen substrate, in the diatom Phaeodactylum tricornutum leads to a metabolic imbalance within the cell
The closest representatives of primary endosymbiotic phototrophs are rhodophytes and glaucophytes branching with fungi, but they possess only the eukaryotic pyrimidinesynthesis associated CPS

Summary

Introduction

Eukaryotic complex phototrophs exhibit a colorful evolutionary history. At least three independent endosymbiotic events accompanied by the gene transfer from the endosymbiont to host assembled a complex genomic mosaic. Metazoans use the OUC as a catabolic pathway (i.e., to metabolize the conversion of toxic ammonia to harmless urea), in stramenopiles, it seems to have rather an anabolic character instead It plays a vital role in the overall cellular balance of carbon and n itrogen[1,2]. Allen et al.[1] showed that the key enzyme of the OUC, carbamoyl phosphate synthase (CPS), has likely evolved by a duplication of an ancient CPS involved in pyrimidine biosynthesis and switch of its substrate specificity from glutamate to ammonium. Apicomplexans use the CPS involved in OUC in animals to produce pyrimidines and lost the original OUC during the evolution This evolutionary scenario is relatively complex, it shows that CPS involved in OUC in animals share common origins with both CPSs homologous enzymes from s tramenopiles[1]

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