Abstract

The order Trypanosomatida has been well studied due to its pathogenicity and the unique biology of the mitochondrion. In Trypanosoma brucei, four DNA polymerases, namely PolIA, PolIB, PolIC, and PolID, related to bacterial DNA polymerase I (PolI), were shown to be localized in mitochondria experimentally. These mitochondrion-localized DNA polymerases are phylogenetically distinct from other family A DNA polymerases, such as bacterial PolI, DNA polymerase gamma (Polγ) in human and yeasts, “plant and protist organellar DNA polymerase (POP)” in diverse eukaryotes. However, the diversity of mitochondrion-localized DNA polymerases in Euglenozoa other than Trypanosomatida is poorly understood. In this study, we discovered putative mitochondrion-localized DNA polymerases in broad members of three major classes of Euglenozoa—Kinetoplastea, Diplonemea, and Euglenida—to explore the origin and evolution of trypanosomatid PolIA-D. We unveiled distinct inventories of mitochondrion-localized DNA polymerases in the three classes: (1) PolIA is ubiquitous across the three euglenozoan classes, (2) PolIB, C, and D are restricted in kinetoplastids, (3) new types of mitochondrion-localized DNA polymerases were identified in a prokinetoplastid and diplonemids, and (4) evolutionarily distinct types of POP were found in euglenids. We finally propose scenarios to explain the inventories of mitochondrion-localized DNA polymerases in Kinetoplastea, Diplonemea, and Euglenida.

Highlights

  • Members of the order Trypanosomatida have been extensively studied because of their pathogenicity to humans

  • 37 family A DNA polymerases were identified in 14 euglenozoan species and subjected to phylogenetic analyses along with their homologs, including Polγ, protist organellar DNA polymerase (POP), and trypanosomatid PolIA–D

  • We found that all the species examined in this study possess sequences that grouped robustly with trypanosomatid PolIA in the global phylogeny of family A DNA polymerases (Figure 1)

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Summary

Introduction

Members of the order Trypanosomatida have been extensively studied because of their pathogenicity to humans. Trypanosoma brucei, Trypanosoma cruzi, and the species belonging to the genus Leishmania cause African trypanosomiasis (sleeping sickness), American trypanosomiasis (Chagas disease), and leishmaniasis, respectively [1]. Besides their significance as the causative agents of deadly diseases, trypanosomatids are important for basic biological research due to the complex architecture of their mitochondrial genomes (mtDNAs) and RNA-editing of mitochondrial transcripts [2]. A single kDNA contains dozens of maxicircles and thousands of minicircles. Maxicircles carry protein-coding genes and ribosomal RNA genes, of which transcripts need to be edited post-transcriptionally by extensive insertions and deletions of uridines with the help of guide RNAs (gRNAs) transcribed from minicircles. In the genus Trypanosoma, phylogenetically diverse DNA polymerases were experimentally shown to be localized in mitochondria;

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