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Evolution of a Morphological Novelty Occurred Before Genome Compaction in a Lineage of Extreme Parasites,” by Karen L

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Evolution of a Morphological Novelty Occurred Before Genome Compaction in a Lineage of Extreme Parasites,” by Karen L Correction EVOLUTION Correction for “Evolution of a morphological novelty occurred before genome compaction in a lineage of extreme parasites,” by Karen L. Haag, Timothy Y. James, Jean-François Pombert, Ronny Larsson, Tobias M. M. Schaer, Dominik Refardt, and Dieter Ebert, which appeared in issue 43, October 28, 2014, of Proc Natl Acad Sci USA (111:15480–15485; first published October 13, 2014; 10.1073/pnas.1410442111). The authors note, “We described a new basal microsporidian, Mitosporidium daphniae gen. et sp. nov. As was noted in our paper, microsporidians are now classified by some workers in Fungi, but they are nonetheless explicitly excluded from the In- ternational Code of Botanical Nomenclature (1). Having pre- viously been considered animal protists, classified among the so- called ‘sporozoans’, microsporidians continue to fall within the remit of the International Code of Zoological Nomenclature (2). Our paper did not meet all of the conditions mandated by the Zoological Code for making their new generic and specific names nomenclaturally available. In particular, no name-bearing type (holotype, syntypes, or hapantotype) was fixed for the new species, and because the specific name was thus unavailable, so was the new generic name, for which fixation of an available type species was also necessary. Here we propose to remedy this sit- uation by again proposing the new taxon Mitosporidium daphniae gen. et sp. nov., with the generic and specific diagnoses as given by Haag et al. and with M. daphniae designated as the type species of Mitosporidium. The type series of M. daphniae consists of two type slides (120309-A-1 and 120309-A-2) bearing hapantotypes, which have been deposited in the International Protozoan Type Slide Collection at the Department of Invertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Suitland, MD, USA, under the registration numbers 1251929 and 1251930, respectively. The new taxon was registered at Zoobank under urn:lsid:zoobank.org:pub:7CBB6A53-224B-426A- A8E1-37DE9E332AC4.” 1. Norvell LL (2011) Fungal nomenclature. 1. Melbourne approves a new Code. Mycotaxon 116(1):481–490. 2. International Commission on Zoological Nomenclature (1999) The Code Online. Available at: iczn.org/iczn/index.jsp. Accessed February 3, 2015. www.pnas.org/cgi/doi/10.1073/pnas.1502848112 E1162 | PNAS | March 10, 2015 | vol. 112 | no. 10 www.pnas.org Downloaded by guest on September 28, 2021 Evolution of a morphological novelty occurred before genome compaction in a lineage of extreme parasites Karen L. Haaga,b,1, Timothy Y. Jamesc, Jean-François Pombertd, Ronny Larssone, Tobias M. M. Schaera, Dominik Refardta,f, and Dieter Eberta aZoological Institute, Basel University, 4051 Basel, Switzerland; bDepartment of Genetics, Federal University of Rio Grande do Sul, Porto Alegre, 91501-970 RS, Brazil; cDepartment of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109; dDepartment of Biological and Chemical Sciences, Illinois Institute of Technology, Chicago, IL 60616; eDepartment of Biology, University of Lund, SE-223 62 Lund, Sweden; and fInstitute of Natural Resource Sciences, Zurich University of Applied Sciences, 8820 Wädenswil, Switzerland Edited by Patrick J. Keeling, University of British Columbia, Vancouver, BC, Canada, and accepted by the Editorial Board September 10, 2014 (receivedfor review June 9, 2014) Intracellular parasitism results in extreme adaptations, whose and oxidative phosphorylation (12, 13). For example, the human evolutionary history is difficult to understand, because the para- parasite Enterocytozoon bieneusi seems to have no fully functional sites and their known free-living relatives are so divergent from pathway to generate ATP from glucose (12), relying on trans- one another. Microsporidia are intracellular parasites of humans porters to import ATP from its host. These ATP transporters have and other animals, which evolved highly specialized morpholog- been acquired by horizontal gene transfer (HGT) from in- ical structures, but also extreme physiologic and genomic simpli- tracellular parasitic bacteria (13). Despite major progress in the fication. They are suggested to be an early-diverging branch on understanding of microsporidian biology, it is still unclear how the fungal tree, but comparisons to other species are difficult this clade of extreme parasites evolved. because their rates of molecular evolution are exceptionally high. The key to understanding the sequence of events leading to Mitochondria in microsporidia have degenerated into organelles extreme parasitism is a well-resolved phylogeny. Microsporidia called mitosomes, which have lost a genome and the ability to produce ATP. Here we describe a gut parasite of the crustacean pose a problem in this regard due to their phenomenal molecular Daphnia that despite having remarkable morphological similarity rate acceleration, possibly related to loss of cell cycle control EVOLUTION to the microsporidia, has retained genomic features of its fungal genes (14). A phylogenetic analysis of 53 conserved concate- ancestors. This parasite, which we name Mitosporidium daphniae nated genes supports a topology in which microsporidia is the gen. et sp. nov., possesses a mitochondrial genome including genes most basal branch in the fungal tree (5). Another phylogenetic for oxidative phosphorylation, yet a spore stage with a highly spe- analysis based on 200 genes included the endoparasite Rozella cialized infection apparatus—the polar tube—uniquely known only allomycis, a representative of the recently discovered basal fungal from microsporidia. Phylogenomics places M. daphniae at the root of lineage Cryptomycota (15, 16), and placed microsporidia and the microsporidia. A comparative genomic analysis suggests that the Cryptomycota together on the most basal fungal branch (4). One reduction in energy metabolism, a prominent feature of microspori- of the shared genomic elements between microsporidia and dian evolution, was preceded by a reduction in the machinery con- R. allomycis is the nucleotide transporter that is used by micro- trolling cell cycle, DNA recombination, repair, and gene expression. sporidia for stealing energy in the form of ATP from their hosts; These data show that the morphological features unique to M. daphniae and other microsporidia were already present before Significance the lineage evolved the extreme host metabolic dependence and loss of mitochondrial respiration for which microsporidia are Intracellular obligate parasitism results in extreme adaptations, well known. whose evolutionary history is difficult to understand, because intermediate forms are hardly ever found. Microsporidia are microsporidia | genome evolution | phylogenomics | highly derived intracellular parasites that are related to fungi. We evolution of extreme parasitism | Daphnia describe the evolutionary history of a new microsporidian para- site found in the hindgut epithelium of the crustacean Daphnia icrosporidia are intracellular parasites that represent the and conclude that the new species has retained ancestral features Mextreme of known genome simplification and size reduction that were lost in other microsporidia, whose hallmarks are the among eukaryotes (1). There are more than 1,200 described evolution of a unique infection apparatus, extreme genome re- microsporidia species (2), with several having an economic im- duction, and loss of mitochondrial respiration. The first evolu- pact by causing disease in animals such as fish and honey bees, tionary steps leading to the extreme metabolic and genomic and are a problem to human health, in particular since the AIDS simplification of microsporidia involved the adoption of a para- pandemic. Microsporidia are currently placed on an ancestral sitic lifestyle, the development of a specialized infection appa- branch within the fungi, although this placement has only recently ratus, and the loss of diverse regulatory proteins. been worked out, due to the absence of clear morphological and physiological connections to other eukaryotes and the profound Author contributions: K.L.H. and D.E. designed research; K.L.H., T.Y.J., J.-F.P., R.L., T.M.M.S., changes resulting from adaptations to an intracellular lifestyle (3– and D.R. performed research; R.L. and D.E. contributed new reagents/analytic tools; K.L.H., T.Y.J., J.-F.P., R.L., and D.E. analyzed data; and K.L.H., T.Y.J., J.-F.P., R.L., and D.E. wrote 6). The evolutionary history of microsporidia is marked by the loss the paper. of several eukaryotic features, such as mitochondria (7), a typical The authors declare no conflict of interest. Golgi apparatus (8), a flagellum (3), and the evolutionary in- This article is a PNAS Direct Submission. P.J.K. is a guest editor invited by the Editorial novation of an infection apparatus, the polar tube. Microsporidia Board. evolved distinctive genetic features, such as massive loss of genes, Data deposition: The sequences reported in this paper have been deposited in the Gen- leading to the smallest known eukaryotic genomes (1). Remnants Bank database for GenBank BioProject PRJNA243305 and BioSample SAMN02714227 of mitochondria appear in microsporidian cells as DNA-free (accession no. JMKJ00000000). organelles called mitosomes (9, 10) that perform simplified ver- 1To whom correspondence should be addressed. Email: [email protected]. sions of the original mitochondrial functions, such as the assembly This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.
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