The trypanosomatid flagellates possess in their single mitochondrion a highly complex kinetoplast (k)DNA, which is composed of interlocked circular molecules of two types. Dozens of maxicircles represent a classical mitochondrial genome, and thousands of minicircles encode guide (g)RNAs, which direct the processive and essential uridine insertion/deletion messenger RNA (mRNA) editing of maxicircle transcripts. While the details of kDNA structure and this type of RNA editing are well established, our knowledge mostly relies on a narrow foray of intensely studied human parasites of the genera Leishmania and Trypanosoma. Here, we analyzed kDNA, its expression, and RNA editing of two members of the poorly characterized genus Vickermania with very different cultivation histories. In both Vickermania species, the gRNA-containing heterogeneous large (HL)-circles are atypically large with multiple gRNAs each. Examination of Vickermania spadyakhi HL-circle loci revealed a massive redundancy of gRNAs relative to the editing needs. In comparison, the HL-circle repertoire of extensively cultivated Vickermania ingenoplastis is greatly reduced. It correlates with V. ingenoplastis-specific loss of productive editing of transcripts encoding subunits of respiratory chain complex I and corresponding lack of complex I activity. This loss in a parasite already lacking genes for subunits of complexes III and IV suggests an apparent requirement for its mitochondrial adenosine triphosphate (ATP) synthase to work in reverse to maintain membrane potential. In contrast, V. spadyakhi retains a functional complex I that allows ATP synthase to work in its standard direction.

Department of Biochemistry Faculty of Natural Sciences Comenius University Bratislava 842 15 Slovakia

Department of Biomedical Sciences University of Minnesota Medical School Duluth MN 55812

Department of Glycobiology Institute of Chemistry Slovak Academy of Sciences Bratislava 845 38 Slovakia

e Duve Institute Université Catholique de Louvain Brussels 1200 Belgium

Faculty of Biology M 5 Lomonosov Moscow State University Moscow 119991 Russia

Faculty of Science University of South Bohemia 370 05 České Budějovice Czechia

Institute of Parasitology Biology Centre Czech Academy of Sciences České Budějovice 370 05 Czechia

Life Science Research Centre Faculty of Science University of Ostrava Ostrava 710 00 Czechia

Medirex Group Academy Nitra 949 05 Slovakia

Université Libre de Bruxelles Gosselies 6041 Belgium

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