Mitochondrial Gene Expression Is Responsive to Starvation Stress and Developmental Transition in Trypanosoma cruzi

Trypanosoma cruzi parasites causing Chagas disease are passed be- tween mammals by the triatomine bug vector. Within the insect, T. cruzi epimastigote-stage cells replicate and progress through the increasingly nutrient- restricted digestive tract, differentiating into infectious, nonreplicative metacyclic try- pomastigotes. Thus, we evaluated how nutrient perturbations or metacyclogenesis affects mitochondrial gene expression in different insect life cycle stages. We com- pared mitochondrial RNA abundances in cultures containing fed, replicating epimas- tigotes, differentiating cultures containing both starved epimastigotes and metacy- clic trypomastigotes and epimastigote starvation cultures. We observed increases in mitochondrial rRNAs and some mRNAs in differentiating cultures. These increases predominated only for the edited CYb mRNA in cultures enriched for metacyclic try- pomastigotes. For the other transcripts, abundance increases were linked to starva- tion and were strongest in culture fractions with a high population of starved epi- mastigotes. We show that loss of both glucose and amino acids results in rapid increases in RNA abundances that are quickly reduced when these nutrients are re- turned. Furthermore, the individual RNAs exhibit distinct temporal abundance pat- terns, suggestive of multiple mechanisms regulating individual transcript abundance. Finally, increases in mitochondrial respiratory complex subunit mRNA abundances were not matched by increases in abundances of nucleus-encoded subunit mRNAs, nor were there statistically significant increases in protein levels of three nucleus- encoded subunits tested. These results show that, similarly to that in T. brucei, the mitochondrial genome in T. cruzi has the potential to alter gene expression in re- sponse to environmental or developmental stimuli but for an as-yet-unknown purpose.