Evolution of a morphological novelty occurred before genome compaction in a lineage of extreme parasites

• Published in: Proceedings of the National Academy of Sciences - PNAS 2014-10, Vol.111 (43), p.15480-15485
• Main Authors: Haag, Karen L., James, Timothy Y., Pombert, Jean-François, Larsson, Ronny, Schaer, Tobias M. M., Refardt, Dominik, Ebert, Dieter
• Format: Article
• Language: English
• Subjects: Animals; Biologi; Biological Sciences; Chitin; Daphnia; Evolution; Evolution, Molecular; Freshwater; Fungi; Genome, Fungal - genetics; Genomes; Genomics; Metabolism; Microsporidia; Microsporidia - genetics; Microsporidia - ultrastructure; Mitochondria; Molecular Sequence Annotation; Molecular Sequence Data; Morphology; Natural Sciences; Naturvetenskap; Parasites; Parasites - anatomy & histology; Parasites - genetics; Parasites - ultrastructure; Phosphorylation; Phylogenetics; Phylogeny; Sequence Analysis, DNA; Species Specificity; Spores; Zoologi; Zoology
• ISSN: 0027-8424; 1091-6490; 1091-6490
• DOI: 10.1073/pnas.1410442111

Significance Intracellular obligate parasitism results in extreme adaptations, whose evolutionary history is difficult to understand, because intermediate forms are hardly ever found. Microsporidia are highly derived intracellular parasites that are related to fungi. We describe the evolutionary history of a new microsporidian parasite found in the hindgut epithelium of the crustacean Daphnia and conclude that the new species has retained ancestral features that were lost in other microsporidia, whose hallmarks are the evolution of a unique infection apparatus, extreme genome reduction, and loss of mitochondrial respiration. The first evolutionary steps leading to the extreme metabolic and genomic simplification of microsporidia involved the adoption of a parasitic lifestyle, the development of a specialized infection apparatus, and the loss of diverse regulatory proteins. Intracellular parasitism results in extreme adaptations, whose evolutionary history is difficult to understand, because the parasites and their known free-living relatives are so divergent from one another. Microsporidia are intracellular parasites of humans and other animals, which evolved highly specialized morphological structures, but also extreme physiologic and genomic simplification. They are suggested to be an early-diverging branch on the fungal tree, but comparisons to other species are difficult because their rates of molecular evolution are exceptionally high. Mitochondria in microsporidia have degenerated into organelles called mitosomes, which have lost a genome and the ability to produce ATP. Here we describe a gut parasite of the crustacean Daphnia that despite having remarkable morphological similarity to the microsporidia, has retained genomic features of its fungal ancestors. This parasite, which we name Mitosporidium daphniae gen. et sp. nov., possesses a mitochondrial genome including genes for oxidative phosphorylation, yet a spore stage with a highly specialized infection apparatus—the polar tube—uniquely known only from microsporidia. Phylogenomics places M. daphniae at the root of the microsporidia. A comparative genomic analysis suggests that the reduction in energy metabolism, a prominent feature of microsporidian evolution, was preceded by a reduction in the machinery controlling cell cycle, DNA recombination, repair, and gene expression. These data show that the morphological features unique to M. daphniae and other microsporidia were already present before t