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.

Center for Computational Sciences University of Tsukuba Tsukuba 305 8577 Japan

Department of Applied Chemistry and Food Science Fukui University of Technology Fukui 910 8505 Japan

Department of Gene Function and Phenomics National Institute of Genetics Mishima 411 8540 Japan

Department of Parasitology Charles University Faculty of Science BIOCEV 252 42 Vestec Czech Republic

Department of Zoology National Museum of Nature and Science Tsukuba 305 0005 Japan

Faculty of Life and Environmental Sciences University of Tsukuba Tsukuba 305 8572 Japan

Graduate School of Engineering Fukui University of Technology Fukui 910 8505 Japan

Graduate School of Life and Environmental Sciences University of Tsukuba Tsukuba 305 8572 Japan

Japan Agency for Marine Earth Science and Technology Yokosuka 236 0001 Japan

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Encyclopedia of Family A DNA Polymerases Localized in Organelles: Evolutionary Contribution of Bacteria Including the Proto-Mitochondrion

Heterotrophic euglenid Rhabdomonas costata resembles its phototrophic relatives in many aspects of molecular and cell biology