Delineating transitions during the evolution of specialised peroxisomes: glycosome formation in kinetoplastid and diplonemid protists

Diego Andrade-Alviárez, Alejandro D. Bonive-Boscan , Ana J. Cáceres, Wilfredo Quiñones, Melisa Gualdrón-López, Michael L. Ginger, Paul Michels*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

Abstract

One peculiarity of protists belonging to classes Kinetoplastea and Diplonemea within the phylum Euglenozoa is compartmentalisation most glycolytic enzymes within peroxisomes that are hence called glycosomes. This pathway is not sequestered in peroxisomes of the third Euglenozoan class, Euglenida. Previous analysis of well-studied representatives of the kinetoplastids, the ‘TriTryps’ parasites Trypanosoma brucei, Trypanosoma cruzi and Leishmania spp. identified within the glycosomes also some other metabolic processes usually not present in peroxisomes. In addition, trypanosomatid peroxins, i.e. proteins involved in biogenesis of these organelles, appeared quite divergent from their human and yeast homologues. In recent years, genome, transcriptome and proteome sequences of a variety of representatives from different euglenozoan classes have become available. We tracked the possible evolution of glycosomes by querying the databases, as well as those of a non-Euglenozoan protist belonging to the same protist supergroup Discoba. We searched for orthologues of TriTryps proteins involved in glycosomal metabolism and biogenesis. Predicted cellular location(s) of each metabolic enzyme identified was inferred from presence or absence of peroxisomal-targeting signals (PTSs). Combined with a survey of relevant literature our study facilitated extensive refinement of our previously postulated hypothesis about glycosome evolution. The data agree glycolysis was compartmentalised in a common ancestor of the kinetoplastids and diplonemids, yet additionally indicates most other processes found in glycosomes of extant trypanosomatids, but not in peroxisomes of other organisms were either sequestered in this ancestor or shortly after separation of the two lineages. Peroxin divergence is evident in all euglenozoans. Following their gain of pathway complexity, subsequent evolution of peroxisome/glycosome function is complex. We hypothesize compartmentalisation in glycosomes of glycolytic enzymes, their cofactors and subsequently other metabolic enzymes provided selective advantage to kinetoplastids and diplonemids during their evolution in changing marine environments. We contend two specific properties derived from the ancestral peroxisomes were key: existence of nonselective pores for small solutes and the possibility of high turnover by pexophagy. Critically, such pores and pexophagy are characterised in extant trypanosomatids. Increasing amenability of free-living kinetoplastids and recently isolated diplonemids to experimental study means our hypothesis and interpretation of bioinformatic data are suited to experimental interrogation.
Original languageEnglish
Article number979269
Number of pages26
JournalFrontiers in Cell and Developmental Biology
Volume10
DOIs
Publication statusPublished - 12 Sep 2022

Keywords

  • Euglenozoa
  • glycosome
  • peroxisome
  • phylogenomics
  • glycolysis
  • metabolic compartmentalisation
  • biogenesis
  • pexophagy

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