The remarkable metabolism of vickermania ingenoplastis: Genomic predictions

Fred R. Opperdoes, Anzhelika Butenko, Alexandra Zakharova, Evgeny S. Gerasimov, Sara L. Zimmer, Julius Lukeš, Vyacheslav Yurchenko

Research output: Contribution to journalArticlepeer-review

Abstract

A recently redescribed two-flagellar trypanosomatid Vickermania ingenoplastis is insensitive to the classical inhibitors of respiration and thrives under anaerobic conditions. Using genomic and transcriptomic data, we analyzed its genes of the core metabolism and documented that subunits of the mitochondrial respiratory complexes III and IV are ablated, while those of complexes I, II, and V are all present, along with an alternative oxidase. This explains the previously reported conversion of glucose to acetate and succinate by aerobic fermentation. Glycolytic pyruvate is metabolized to acetate and ethanol by pyruvate dismutation, whereby a unique type of alcohol dehydrogenase (shared only with Phytomonas spp.) processes an excess of reducing equivalents formed under anaerobic conditions, leading to the formation of ethanol. Succinate (formed to maintain the glycosomal redox balance) is converted to propionate by a cyclic process involving three enzymes of the mitochondrial methyl-malonyl-CoA pathway, via a cyclic process, which results in the formation of additional ATP. The unusual structure of the V. ingenoplastis genome and its similarity with that of Phytomonas spp. imply their relatedness or convergent evolution. Nevertheless, a critical difference between these two trypanosomatids is that the former has significantly increased its genome size by gene duplications, while the latter streamlined its genome.

Original languageEnglish (US)
Article number68
Pages (from-to)1-12
Number of pages12
JournalPathogens
Volume10
Issue number1
DOIs
StatePublished - Jan 14 2021

Bibliographical note

Funding Information:
This research was funded by the European Regional Funds (CZ.02.1.01/16_019/0000759), the Grant Agency of Czech Republic (20-07186S and 21-09283S) to V.Y. and J.L., the ERC CZ (LL1601) to J.L., and the University of Ostrava (SGS/PrF/2021) to A.Z. Two specific tasks were funded by the Russian Science Foundation grants 19-15-00054 for analysis of orthologues of Leishmania major genes to V.Y. and 19-74-10008 for whole-transcriptome analysis of kinetoplast-encoded gene expression to E.S.G. F.R.O. received support from the de Duve Institute.

Keywords

  • Genome sequencing
  • Metabolism
  • Phytomonas
  • Vickermania ingenoplastis

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