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

Haag, Karen L; James, Timothy Y; Pombert, Jean-François; Larsson, Ronny LU ; Schaer, Tobias M M; Refardt, Dominik and Ebert, Dieter (2014) In Proceedings of the National Academy of Sciences 111(43). p.15480-15485
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... (More)
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. (Less)
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Contribution to journal
publication status
published
subject
in
Proceedings of the National Academy of Sciences
volume
111
issue
43
pages
15480 - 15485
publisher
National Acad Sciences
external identifiers
  • pmid:25313038
  • wos:000343729500058
  • scopus:84908296286
ISSN
1091-6490
DOI
10.1073/pnas.1410442111
language
English
LU publication?
yes
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db9ce757-83db-4f59-99de-e7b8cfd5ae7c (old id 4736980)
date added to LUP
2014-11-10 13:36:44
date last changed
2017-10-01 03:27:04
@article{db9ce757-83db-4f59-99de-e7b8cfd5ae7c,
  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.},
  author       = {Haag, Karen L and James, Timothy Y and Pombert, Jean-François and Larsson, Ronny and Schaer, Tobias M M and Refardt, Dominik and Ebert, Dieter},
  issn         = {1091-6490},
  language     = {eng},
  number       = {43},
  pages        = {15480--15485},
  publisher    = {National Acad Sciences},
  series       = {Proceedings of the National Academy of Sciences},
  title        = {Evolution of a morphological novelty occurred before genome compaction in a lineage of extreme parasites.},
  url          = {http://dx.doi.org/10.1073/pnas.1410442111},
  volume       = {111},
  year         = {2014},
}