The canonical stop codons of the nuclear genome of the trypanosomatid Blastocrithidia nonstop are recoded. Here, we investigated the effect of this recoding on the mitochondrial genome and gene expression. Trypanosomatids possess a single mitochondrion and protein-coding transcripts of this genome require RNA editing in order to generate open reading frames of many transcripts encoded as 'cryptogenes'. Small RNAs that can number in the hundreds direct editing and produce a mitochondrial transcriptome of unusual complexity. We find B. nonstop to have a typical trypanosomatid mitochondrial genetic code, which presumably requires the mitochondrion to disable utilization of the two nucleus-encoded suppressor tRNAs, which appear to be imported into the organelle. Alterations of the protein factors responsible for mRNA editing were also documented, but they have likely originated from sources other than B. nonstop nuclear genome recoding. The population of guide RNAs directing editing is minimal, yet virtually all genes for the plethora of known editing factors are still present. Most intriguingly, despite lacking complex I cryptogene guide RNAs, these cryptogene transcripts are stochastically edited to high levels.

De Duve Institute Université Catholique de Louvain 1200 Brussels Belgium

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

Department of Parasitology Faculty of Science Charles University BIOCEV 252 50 Vestec Czechia

Division of Infectious Diseases Department of Medicine University of Alberta T6G 2R3 Edmonton Alberta Canada

Faculty of Biology Lomonosov Moscow State University Moscow 119991 Russia

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

Institute for Information Transmission Problems Russian Academy of Sciences Moscow 127051 Russia

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

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

University of Minnesota Medical School Duluth Campus Duluth MN 55812 USA

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