The mitochondrial genome of Toxoplasma gondii is highly fragmented and recombination-prone, creating a structurally dynamic genetic landscape. How such a genome is used efficiently to produce functional mRNAs remains unclear: it is unknown whether transcription draws from many alternative genomic configurations or a restricted subset, and how any resulting precursor RNAs are processed into mature transcripts. More broadly, mitochondrial RNA processing mechanisms in this system are poorly understood. Here, we show that recombination of the T. gondii mitochondrial genome generates a diverse population of structurally distinct precursor RNAs for the essential cytochrome c oxidase subunit I (coxI) protein. Rather than being derived from a single defined primary transcript, these heterogeneous precursors are unified into a single mature mRNA through a post-transcriptional mechanism dependent on the DEAD-box RNA helicase TgmRHel. TgmRHel is required for 5'-end processing of coxI mRNA and for the accumulation of mitochondrial rRNAs, both of which are essential for Complex IV biogenesis, oxidative phosphorylation, and parasite survival. Loss of TgmRHel leads to the accumulation of diverse coxI precursor RNAs and a failure to generate the mature transcript. Our findings reveal an unexpected genome-transcriptome interface in which extensive genomic variability is not suppressed at the DNA level but instead resolved through RNA helicase-mediated processing. This work establishes a new conceptual framework for how gene expression fidelity can be maintained in the context of highly dynamic, recombining genomes.
Gluhic, Z., Tetzlaff, S., Liebers, P., Drakoulis, N., Possling, A., Maguire, C. S., Flores, V., Waller, R., van Dooren, G., Schmitz-Linneweber, C.
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