Mitochondrial genomes in Perkinsus decode conserved frameshifts in all genes

Sebastian G. Gornik, Victor Flores, Franziska Reinhardt, Lieselotte Erber, Dayana E Salas-Leiva, Olga Douvropoulou, Imen Lassadi, Elin Einarsson, Mario Mörl, Anna Git, Peter F Stadler, Arnab Pain, Ross F Waller

Research output: Contribution to journalArticlepeer-review

Abstract

Mitochondrial genomes of apicomplexans, dinoflagellates and chrompodellids that collectively make up the Myzozoa, encode only three proteins (COB, COX1, COX3), contain fragmented rRNAs, and display extensive recombination, RNA trans-splicing, and RNA-editing. The early-diverging Perkinsozoa is the final major myzozoan lineage whose mitochondrial genomes remained poorly characterized. Previous reports of Perkinsus genes indicated independent acquisition of non-canonical features, namely the occurrence of multiple frameshifts. To determine both ancestral myzozoan and novel perkinsozoan mitochondrial genome features, we sequenced and assembled mitochondrial genomes of four Perkinsus species. These data show a simple ancestral genome with the common reduced coding capacity but disposition for rearrangement. We identified 75 frameshifts across the four species that occur as distinct types and that are highly conserved in gene location. A decoding mechanism apparently employs unused codons at the frameshift sites that advance translation either +1 or +2 frames to the next used codon. The locations of frameshifts are seemingly positioned to regulate protein folding of the nascent protein as it emerges from the ribosome. cox3 is distinct in containing only one frameshift and showing strong selection against residues that are otherwise frequently encoded at the frameshift positions in cox1 and cob. All genes lack cysteine codons implying a reduction to 19 amino acids in these genomes. Furthermore, mitochondrion-encoded rRNA fragment complements are incomplete in Perkinsus spp. but some are found in the nuclear DNA suggesting import into the organelle. Perkinsus demonstrates further remarkable trajectories of organelle genome evolution including pervasive integration of frameshift translation into genome expression.
Original languageEnglish (US)
JournalMolecular Biology and Evolution
DOIs
StatePublished - Sep 15 2022

Bibliographical note

KAUST Repository Item: Exported on 2022-09-19
Acknowledged KAUST grant number(s): BAS/1/1020-01-01
Acknowledgements: This work was supported by grants from the Gordon and Betty Moore Foundation (GBMF9194), Australian Research Council (DP130100572), the King Abdullah University of Science and Technology (KAUST; BAS/1/1020-01-01) and the Deutsche For schungsgemeinschaft (DFG; MO 634/21-1, MO 634/8- 2 and INST 268/413-1). We also thank Fathia Ben Rached, Sara Mfarrej and Amit K. Subudhi of KAUST for helping with culturing and Perkinsus DNA extractions.

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Genetics
  • Molecular Biology

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