Comparative molecular cell biology of phototrophic euglenids and parasitic trypanosomatids sheds light on the ancestor of Euglenozoa

Abstract

Parasitic trypanosomatids and phototrophic euglenids are among the most extensively studied euglenozoans. The phototrophic euglenid lineage arose relatively recently through secondary endosymbiosis between a phagotrophic euglenid and a prasinophyte green alga that evolved into the euglenid secondary chloroplast. The parasitic trypanosomatids (i.e. Trypanosoma spp. and Leishmania spp.) and the freshwater phototrophic euglenids (i.e. Euglena gracilis) are the most evolutionary distant lineages in the Euglenozoa phylogenetic tree. The molecular and cell biological traits they share can thus be considered as ancestral traits originating in the common euglenozoan ancestor. These euglenozoan ancestral traits include common mitochondrial presequence motifs, respiratory chain complexes containing various unique subunits, a unique ATP synthase structure, the absence of mitochondria‐encoded transfer RNAs (tRNAs), a nucleus with a centrally positioned nucleolus, closed mitosis without dissolution of the nuclear membrane and nucleoli, a nuclear genome containing the unusual ‘J’ base (β‐D‐glucosyl‐hydroxymethyluracil), processing of nucleus‐encoded precursor messenger RNAs (pre‐mRNAs) via spliced‐leader RNA (SL‐RNA) trans‐splicing, post‐transcriptional gene silencing by the RNA interference (RNAi) pathway and the absence of transcriptional regulation of nuclear gene expression. Mitochondrial uridine insertion/deletion RNA editing directed by guide RNAs (gRNAs) evolved in the ancestor of the kinetoplastid lineage. The evolutionary origin of other molecular features known to be present only in either kinetoplastids (i.e. polycistronic transcripts, compaction of nuclear genomes) or euglenids (i.e. monocistronic transcripts, huge genomes, many nuclear cis‐spliced introns, polyproteins) is unclear.

A Uniquely Complex Mitochondrial Proteome from Euglena gracilis

“…2016 ), and Kinetoplastea, a group notable for numerous parasite members of public health importance ( Gibson 2017 ). From an evolutionary perspective, the extensively studied kinetoplastids are more distant to euglenids than diplonemids ( Vesteg et al. 2019 ).…”

N- and O-Glycosylation Pathways in the Microalgae Polyphyletic Group

“…In addition, a few photosynthetic unicellular organisms are belonging to other Eukaryotic supergroups. For example, the Euglenid group, belonging to the Excavate supergroup, encompasses several freshwater and marine or brackish phototrophic species that are spread out in Euglenales and Eutreptiales, respectively (Vesteg et al, 2019). These phototrophic species are thought to have emerged recently (about 600 million years ago) as the result of a secondary endosymbiosis between an Euglenid host cell and a prasinophyte green alga (Jackson et al, 2018).…”

De Novo Transcriptome Meta-Assembly of the Mixotrophic Freshwater Microalga Euglena gracilis

“…Owing to its singular evolutionary origin, a merger between a chlorophyte alga and a phagotrophic unicellular belonging to a non-model eukaryotic group [20], E. gracilis is a fascinating, multifaceted chimeric organism, whose significance is constantly growing in domains as varied as the production of bio-based products [43], the treatment of wastewater ( [130]), the provision of food supplements for space exploration [131], or the elucidation of mechanisms it shares with its parasitic trypanosome cousins [8,9,15] (see also the other articles of the present Special Issue).…”

“…Beyond the technical issues that may have contributed to a loss of exploitable signal (e.g., heterogeneous experimental "design", see Table 1, uncorrected batch effects), these negative results can also be interpreted as additional evidence for the idea that, similar to what is known in trypanosomatids, nuclear gene expression in E. gracilis is not primarily regulated at the transcriptional level. In these parasites, gene regulation mostly occurs at the post-transcriptional level, through stabilization/degradation of mRNA molecules and control of mRNA translation (see [8] for a recent review of the issue). While the former mechanism should in principle change transcript abundance, the latter one might not be visible in comparative transcriptomics.…”

“…Euglenids are early diverged members of the Euglenozoa and distant relatives to the kinetoplastids [6]. Thus, analysing E. gracilis genomic information is a way to approach the evolution of parasitism, due to their common ancestry with kinetoplastids [7,8]. For example, it has been shown that many additional subunits of the mitochondrial respiratory chain previously considered exclusive to kinetoplastids are shared with E. gracilis, and therefore cannot be associated with the parasitic lifestyle [9].…”