title: Evolution of a morphological novelty occurred before genome compaction in a lineage of extreme parasites.
abstract: 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 the lineage evolved the extreme host metabolic dependence and loss of mitochondrial respiration for which microsporidia are well known.
authors.affiliation: Zoological Institute, Basel University, 4051 Basel, Switzerland; Department of Genetics, Federal University of Rio Grande do Sul, Porto Alegre, 91501-970 RS, Brazil; karen.haag@ufrgs.br.
authors.forename: Karen L
authors.initials: KL
authors.lastname: Haag
authors.affiliation: Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109;
authors.forename: Timothy Y
authors.initials: TY
authors.lastname: James
authors.affiliation: Department of Biological and Chemical Sciences, Illinois Institute of Technology, Chicago, IL 60616;
authors.forename: Jean-François
authors.initials: JF
authors.lastname: Pombert
authors.affiliation: Department of Biology, University of Lund, SE-223 62 Lund, Sweden; and.
authors.forename: Ronny
authors.initials: R
authors.lastname: Larsson
authors.affiliation: Zoological Institute, Basel University, 4051 Basel, Switzerland;
authors.forename: Tobias M M
authors.initials: TM
authors.lastname: Schaer
authors.affiliation: Zoological Institute, Basel University, 4051 Basel, Switzerland; Institute of Natural Resource Sciences, Zurich University of Applied Sciences, 8820 Wädenswil, Switzerland.
authors.forename: Dominik
authors.initials: D
authors.lastname: Refardt
authors.affiliation: Zoological Institute, Basel University, 4051 Basel, Switzerland;
authors.forename: Dieter
authors.initials: D
authors.lastname: Ebert
mesh_terms: D000818:Animals; D019143:Evolution, Molecular; D016681:Genome, Fungal / Q000235:genetics*; D023281:Genomics; D016814:Microsporidia / Q000235:genetics* / Q000648:ultrastructure; D058977:Molecular Sequence Annotation; D008969:Molecular Sequence Data; D010271:Parasites / Q000033:anatomy & histology* / Q000235:genetics* / Q000648:ultrastructure; D010802:Phylogeny; D017422:Sequence Analysis, DNA; D013045:Species Specificity
keywords: Daphnia; evolution of extreme parasitism; genome evolution; microsporidia; phylogenomics