| Summary: | Euglenozoa comprises euglenids, kinetoplastids, and diplonemids, with
each group exhibiting different and highly unusual mitochondrial genome
organizations. Although they are sister groups, kinetoplastids and diplonemids have very distinct mitochondrial genome architectures, requiring
widespread insertion/deletion RNA editing and extensive trans-splicing,
respectively, in order to generate functional transcripts. The evolutionary
history by which these differing processes arose remains unclear. Using
single-cell genomics, followed by small sub unit ribosomal DNA and multigene phylogenies, we identified an isolated marine cell that branches on
phylogenetic trees as a sister to known kinetoplastids. Analysis of singlecell amplified genomic material identified multiple mitochondrial genome
contigs. These revealed a gene architecture resembling that of diplonemid
mitochondria, with small fragments of genes encoded out of order and or
on different contigs, indicating that these genes require extensive trans-splicing. Conversely, no requirement for kinetoplastid-like insertion/deletion
RNA-editing was detected. Additionally, while we identified some proteins
so far only found in kinetoplastids, we could not unequivocally identify
mitochondrial RNA editing proteins. These data invite the hypothesis that
extensive genome fragmentation and trans-splicing were the ancestral
states for the kinetoplastid-diplonemid clade but were lost during the kinetoplastid radiation. This study demonstrates that single-cell approaches can
successfully retrieve lineages that represent important new branches on the
tree of life, and thus can illuminate major evolutionary and functional transitions in eukaryotes.
This article is part of a discussion meeting issue ‘Single cell ecology’.
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