Blastocrithidia nonstop mitochondrial genome and its expression are remarkably insulated from nuclear codon reassignment

Author:

Afonin Dmitry A1ORCID,Gerasimov Evgeny S12ORCID,Škodová-Sveráková Ingrid345ORCID,Záhonová Kristína3567ORCID,Gahura Ondřej5ORCID,Albanaz Amanda T S3ORCID,Myšková Eva5,Bykova Anastassia3,Paris Zdeněk58ORCID,Lukeš Julius58ORCID,Opperdoes Fred R9ORCID,Horváth Anton4ORCID,Zimmer Sara L10ORCID,Yurchenko Vyacheslav3ORCID

Affiliation:

1. Faculty of Biology, Lomonosov Moscow State University , Moscow  119991 , Russia

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

3. Life Science Research Centre, Faculty of Science, University of Ostrava , 710 00  Ostrava , Czechia

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

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

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

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

8. Faculty of Science, University of South Bohemia , 370 05  České Budějovice , Czechia

9. De Duve Institute, Université Catholique de Louvain , 1200  Brussels , Belgium

10. University of Minnesota Medical School, Duluth Campus , Duluth , MN  55812 , USA

Abstract

Abstract 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.

Funder

Czech Republic

Russian Science Foundation

University of Ostrava

Ministry of Education

ERDF

Slovak Ministry of Education

Academy of Sciences

Slovak Research and Development Agency

Ministry of Education, Youth and Sports of the Czech Republic

Just Transition

Publisher

Oxford University Press (OUP)

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