Functional consequences of reductive protein evolution in a minimal eukaryotic genome

Microsporidia are parasites with the smallest known eukaryotic genomes. Taking a comparative genomic approach, we identified microsporidia orthologs of budding yeast proteins and show that the median microsporidia protein is 21% shorter than its yeast counterpart. Microsporidia proteins are shorter due to reduced domain lengths, diminished linker lengths, and domain loss. On average, 34% of microsporidia orthologs have lost C-terminal residues essential for function in yeast, including 13 essential domains lost per genome. Using yeast complementation assays, we show that most microsporidia proteins cannot complement their yeast orthologs, and the ability to complement is about 3-fold less than that observed for the orthologs of Rozella allomycis, a relative of microsporidia. Microsporidia proteins that do not complement are shorter in length than their yeast orthologs. Altogether, our results demonstrate the drastic reduction of microsporidia proteins and show that these reductions have resulted in a diminished ability to function within the context of yeast.