Self-splicing introns are mobile elements that have invaded a number of highly
conserved genes in prokaryotic and organellar genomes. Here, we show that deletion of these
selfish elements from the Saccharomyces cerevisiae mitochondrial genome is stressful to the host.
A strain without mitochondrial introns displays hallmarks of the retrograde response, with altered
mitochondrial morphology, gene expression and metabolism impacting growth and lifespan.
Deletion of the complete suite of mitochondrial introns is phenocopied by overexpression of the
splicing factor Mss116. We show that, in both cases, abnormally efficient transcript maturation
results in excess levels of mature cob and cox1 host mRNA. Thus, inefficient splicing has become
an integral part of normal mitochondrial gene expression. We propose that the persistence of S.
cerevisiae self-splicing introns has been facilitated by an evolutionary lock-in event, where the host
genome adapted to primordial invasion in a way that incidentally rendered subsequent intron loss
deleterious.