TY - JOUR
T1 - A single-cell genome reveals diplonemidlike ancestry of kinetoplastid mitochondrial gene structure
AU - Wideman, Jeremy G.
AU - Lax, Gordon
AU - Leonard, Guy
AU - Milner, David S.
AU - Rodríguez-Martínez, Raquel
AU - Simpson, Alastair G.B.
AU - Richards, Thomas A.
N1 - Funding Information:
and Prokinetoplastina (represented by Perkinsela sp.) and was supported by 76% BS/86% UFB (Metakinetoplastina was fully supported). Diplonemids and euglenids were each recovered with full support, as was the bipartition between Euglenozoa and the other members of Discoba (figure 2).
Publisher Copyright:
© 2019 The Author(s) Published by the Royal Society.
PY - 2019/11/25
Y1 - 2019/11/25
N2 - 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.
AB - 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.
KW - Diplonemids
KW - Evolution
KW - Kinetoplastids
KW - Mitochondrial genome
KW - Single-cell genomics
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U2 - 10.1098/rstb.2019.0100
DO - 10.1098/rstb.2019.0100
M3 - Article
C2 - 31587636
AN - SCOPUS:85072940012
VL - 374
JO - Philosophical Transactions of the Royal Society B: Biological Sciences
JF - Philosophical Transactions of the Royal Society B: Biological Sciences
SN - 0800-4622
IS - 1786
M1 - 20190100
ER -