Crossref journal-article
Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences (341)
Abstract

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.

Bibliography

Haag, K. L., James, T. Y., Pombert, J.-F., Larsson, R., Schaer, T. M. M., Refardt, D., & Ebert, D. (2014). Evolution of a morphological novelty occurred before genome compaction in a lineage of extreme parasites. Proceedings of the National Academy of Sciences, 111(43), 15480–15485.

Authors 7
  1. Karen L. Haag (first)
  2. Timothy Y. James (additional)
  3. Jean-François Pombert (additional)
  4. Ronny Larsson (additional)
  5. Tobias M. M. Schaer (additional)
  6. Dominik Refardt (additional)
  7. Dieter Ebert (additional)
References 47 Referenced 115
  1. N Corradi, J-F Pombert, L Farinelli, ES Didier, PJ Keeling, The complete sequence of the smallest known nuclear genome from the microsporidian Encephalitozoon intestinalis. Nat Commun 1, 77 (2010). (10.1038/ncomms1082) / Nat Commun / The complete sequence of the smallest known nuclear genome from the microsporidian Encephalitozoon intestinalis by Corradi N (2010)
  2. A Mathis, Microsporidia: Emerging advances in understanding the basic biology of these unique organisms. Int J Parasitol 30, 795–804 (2000). (10.1016/S0020-7519(00)00064-3) / Int J Parasitol / Microsporidia: Emerging advances in understanding the basic biology of these unique organisms by Mathis A (2000)
  3. TY James, , Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature 443, 818–822 (2006). (10.1038/nature05110) / Nature / Reconstructing the early evolution of Fungi using a six-gene phylogeny by James TY (2006)
  4. TY James, , Shared signatures of parasitism and phylogenomics unite Cryptomycota and microsporidia. Curr Biol 23, 1548–1553 (2013). (10.1016/j.cub.2013.06.057) / Curr Biol / Shared signatures of parasitism and phylogenomics unite Cryptomycota and microsporidia by James TY (2013)
  5. S Capella-Gutiérrez, M Marcet-Houben, T Gabaldón, Phylogenomics supports microsporidia as the earliest diverging clade of sequenced fungi. BMC Biol 10, 47 (2012). (10.1186/1741-7007-10-47) / BMC Biol / Phylogenomics supports microsporidia as the earliest diverging clade of sequenced fungi by Capella-Gutiérrez S (2012)
  6. N Corradi, PJ Keeling, Microsporidia: A journey through radical taxonomical revisions. Fungal Biol Rev 23, 1–8 (2009). (10.1016/j.fbr.2009.05.001) / Fungal Biol Rev / Microsporidia: A journey through radical taxonomical revisions by Corradi N (2009)
  7. TM Embley, W Martin, Eukaryotic evolution, changes and challenges. Nature 440, 623–630 (2006). (10.1038/nature04546) / Nature / Eukaryotic evolution, changes and challenges by Embley TM (2006)
  8. GV Beznoussenko, , Analogs of the Golgi complex in microsporidia: Structure and avesicular mechanisms of function. J Cell Sci 120, 1288–1298 (2007). (10.1242/jcs.03402) / J Cell Sci / Analogs of the Golgi complex in microsporidia: Structure and avesicular mechanisms of function by Beznoussenko GV (2007)
  9. BAP Williams, RP Hirt, JM Lucocq, TM Embley, A mitochondrial remnant in the microsporidian Trachipleistophora hominis. Nature 418, 865–869 (2002). (10.1038/nature00949) / Nature / A mitochondrial remnant in the microsporidian Trachipleistophora hominis by Williams BAP (2002)
  10. T Cavalier-Smith, Eukaryotes with no mitochondria. Nature 326, 332–333 (1987). (10.1038/326332a0) / Nature / Eukaryotes with no mitochondria by Cavalier-Smith T (1987)
  11. AV Goldberg, , Localization and functionality of microsporidian iron-sulphur cluster assembly proteins. Nature 452, 624–628 (2008). (10.1038/nature06606) / Nature / Localization and functionality of microsporidian iron-sulphur cluster assembly proteins by Goldberg AV (2008)
  12. PJ Keeling, , The reduced genome of the parasitic microsporidian Enterocytozoon bieneusi lacks genes for core carbon metabolism. Genome Biol Evol 2, 304–309 (2010). (10.1093/gbe/evq022) / Genome Biol Evol / The reduced genome of the parasitic microsporidian Enterocytozoon bieneusi lacks genes for core carbon metabolism by Keeling PJ (2010)
  13. AD Tsaousis, , A novel route for ATP acquisition by the remnant mitochondria of Encephalitozoon cuniculi. Nature 453, 553–556 (2008). (10.1038/nature06903) / Nature / A novel route for ATP acquisition by the remnant mitochondria of Encephalitozoon cuniculi by Tsaousis AD (2008)
  14. CA Cuomo, , Microsporidian genome analysis reveals evolutionary strategies for obligate intracellular growth. Genome Res 22, 2478–2488 (2012). (10.1101/gr.142802.112) / Genome Res / Microsporidian genome analysis reveals evolutionary strategies for obligate intracellular growth by Cuomo CA (2012)
  15. MDM Jones, , Discovery of novel intermediate forms redefines the fungal tree of life. Nature 474, 200–203 (2011). (10.1038/nature09984) / Nature / Discovery of novel intermediate forms redefines the fungal tree of life by Jones MDM (2011)
  16. E Lara, D Moreira, P López-García, The environmental clade LKM11 and Rozella form the deepest branching clade of fungi. Protist 161, 116–121 (2010). (10.1016/j.protis.2009.06.005) / Protist / The environmental clade LKM11 and Rozella form the deepest branching clade of fungi by Lara E (2010)
  17. D Ebert Ecology Epidemiology and Evolution of Parasitism in Daphnia. Available at: www.ncbi.nlm.nih.gov/books/NBK2036/. Accessed October 23 2012. (2005).
  18. R Larsson, A new microsporidium Berwaldia singularis gen. et sp.nov. from Daphnia pulex and a survey of microsporidia described from Cladocera. Parasitology 83, 325–342 (1981). (10.1017/S0031182000085334) / Parasitology / A new microsporidium Berwaldia singularis gen. et sp.nov. from Daphnia pulex and a survey of microsporidia described from Cladocera by Larsson R (1981)
  19. D Refardt, D Ebert, The impact of infection on host competition and its relationship to parasite persistence in a Daphnia microparasite system. Evol Ecol 26, 95–107 (2012). (10.1007/s10682-011-9487-5) / Evol Ecol / The impact of infection on host competition and its relationship to parasite persistence in a Daphnia microparasite system by Refardt D (2012)
  20. E Heinz, , The genome of the obligate intracellular parasite Trachipleistophora hominis: New insights into microsporidian genome dynamics and reductive evolution. PLoS Pathog 8, e1002979 (2012). (10.1371/journal.ppat.1002979) / PLoS Pathog / The genome of the obligate intracellular parasite Trachipleistophora hominis: New insights into microsporidian genome dynamics and reductive evolution by Heinz E (2012)
  21. H Shimodaira, An approximately unbiased test of phylogenetic tree selection. Syst Biol 51, 492–508 (2002). (10.1080/10635150290069913) / Syst Biol / An approximately unbiased test of phylogenetic tree selection by Shimodaira H (2002)
  22. L Salichos, A Rokas, Inferring ancient divergences requires genes with strong phylogenetic signals. Nature 497, 327–331 (2013). (10.1038/nature12130) / Nature / Inferring ancient divergences requires genes with strong phylogenetic signals by Salichos L (2013)
  23. J Vávra, J Lukeš Advances in Parasitology, ed D Rollinson (Academic Press, New York), pp. 253–319 (2013). / Advances in Parasitology by Vávra J (2013)
  24. M Valach, , Evolution of linear chromosomes and multipartite genomes in yeast mitochondria. Nucleic Acids Res 39, 4202–4219 (2011). (10.1093/nar/gkq1345) / Nucleic Acids Res / Evolution of linear chromosomes and multipartite genomes in yeast mitochondria by Valach M (2011)
  25. C Roncero, The genetic complexity of chitin synthesis in fungi. Curr Genet 41, 367–378 (2002). (10.1007/s00294-002-0318-7) / Curr Genet / The genetic complexity of chitin synthesis in fungi by Roncero C (2002)
  26. J Ruiz-Herrera, L Ortiz-Castellanos, Analysis of the phylogenetic relationships and evolution of the cell walls from yeasts and fungi. FEMS Yeast Res 10, 225–243 (2010). (10.1111/j.1567-1364.2009.00589.x) / FEMS Yeast Res / Analysis of the phylogenetic relationships and evolution of the cell walls from yeasts and fungi by Ruiz-Herrera J (2010)
  27. A Sebé-Pedrós, X Grau-Bové, TA Richards, I Ruiz-Trillo, Evolution and classification of myosins, a paneukaryotic whole-genome approach. Genome Biol Evol 6, 290–305 (2014). (10.1093/gbe/evu013) / Genome Biol Evol / Evolution and classification of myosins, a paneukaryotic whole-genome approach by Sebé-Pedrós A (2014)
  28. M Schuster, , Myosin-5, kinesin-1 and myosin-17 cooperate in secretion of fungal chitin synthase. EMBO J 31, 214–227 (2012). (10.1038/emboj.2011.361) / EMBO J / Myosin-5, kinesin-1 and myosin-17 cooperate in secretion of fungal chitin synthase by Schuster M (2012)
  29. Y Xu, LM Weiss, The microsporidian polar tube: A highly specialised invasion organelle. Int J Parasitol 35, 941–953 (2005). (10.1016/j.ijpara.2005.04.003) / Int J Parasitol / The microsporidian polar tube: A highly specialised invasion organelle by Xu Y (2005)
  30. SA Karpov, , Morphology, phylogeny, and ecology of the aphelids (Aphelidea, Opisthokonta) and proposal for the new superphylum Opisthosporidia. Front Microbiol 5, 112 (2014). (10.3389/fmicb.2014.00112) / Front Microbiol / Morphology, phylogeny, and ecology of the aphelids (Aphelidea, Opisthokonta) and proposal for the new superphylum Opisthosporidia by Karpov SA (2014)
  31. LK Fritz-Laylin, , The genome of Naegleria gruberi illuminates early eukaryotic versatility. Cell 140, 631–642 (2010). (10.1016/j.cell.2010.01.032) / Cell / The genome of Naegleria gruberi illuminates early eukaryotic versatility by Fritz-Laylin LK (2010)
  32. N Tanaka, S Shuman, RtcB is the RNA ligase component of an Escherichia coli RNA repair operon. J Biol Chem 286, 7727–7731 (2011). (10.1074/jbc.C111.219022) / J Biol Chem / RtcB is the RNA ligase component of an Escherichia coli RNA repair operon by Tanaka N (2011)
  33. L Reiser, P Sánchez-Baracaldo, S Hake, Knots in the family tree: Evolutionary relationships and functions of knox homeobox genes. Plant Mol Biol 42, 151–166 (2000). (10.1023/A:1006384122567) / Plant Mol Biol / Knots in the family tree: Evolutionary relationships and functions of knox homeobox genes by Reiser L (2000)
  34. B Martinac, Mechanosensitive ion channels: Molecules of mechanotransduction. J Cell Sci 117, 2449–2460 (2004). (10.1242/jcs.01232) / J Cell Sci / Mechanosensitive ion channels: Molecules of mechanotransduction by Martinac B (2004)
  35. H Wang, , The multiprotein exocyst complex is essential for cell separation in Schizosaccharomyces pombe. Mol Biol Cell 13, 515–529 (2002). (10.1091/mbc.01-11-0542) / Mol Biol Cell / The multiprotein exocyst complex is essential for cell separation in Schizosaccharomyces pombe by Wang H (2002)
  36. L Cao, , The ancient function of RB-E2F pathway: Insights from its evolutionary history. Biol Direct 5, 55 (2010). (10.1186/1745-6150-5-55) / Biol Direct / The ancient function of RB-E2F pathway: Insights from its evolutionary history by Cao L (2010)
  37. E Peyretaillade, , Identification of transcriptional signals in Encephalitozoon cuniculi widespread among Microsporidia phylum: Support for accurate structural genome annotation. BMC Genomics 10, 607 (2009). (10.1186/1471-2164-10-607) / BMC Genomics / Identification of transcriptional signals in Encephalitozoon cuniculi widespread among Microsporidia phylum: Support for accurate structural genome annotation by Peyretaillade E (2009)
  38. E Peyretaillade, , Annotation of microsporidian genomes using transcriptional signals. Nat Commun 3, 1137 (2012). (10.1038/ncomms2156) / Nat Commun / Annotation of microsporidian genomes using transcriptional signals by Peyretaillade E (2012)
  39. AM Schurko, Jr JM Logsdon, Using a meiosis detection toolkit to investigate ancient asexual “scandals” and the evolution of sex. BioEssays 30, 579–589 (2008). (10.1002/bies.20764) / BioEssays / Using a meiosis detection toolkit to investigate ancient asexual “scandals” and the evolution of sex by Schurko AM (2008)
  40. EI Hazard, T Fukuda, JJ Becnel, Gametogenesis and plasmogamy in certain species of Microspora. J Invertebr Pathol 46, 63–69 (1985). (10.1016/0022-2011(85)90130-2) / J Invertebr Pathol / Gametogenesis and plasmogamy in certain species of Microspora by Hazard EI (1985)
  41. EU Canning, Nuclear division and chromosome cycle in microsporidia. Biosystems 21, 333–340 (1988). (10.1016/0303-2647(88)90030-5) / Biosystems / Nuclear division and chromosome cycle in microsporidia by Canning EU (1988)
  42. YI Wolf, IV Gopich, DJ Lipman, EV Koonin, Relative contributions of intrinsic structural-functional constraints and translation rate to the evolution of protein-coding genes. Genome Biol Evol 2, 190–199 (2010). (10.1093/gbe/evq010) / Genome Biol Evol / Relative contributions of intrinsic structural-functional constraints and translation rate to the evolution of protein-coding genes by Wolf YI (2010)
  43. A Wagner The Origins of Evolutionary Innovations: A Theory of Transformative Change in Living Systems (Oxford Univ Press, Oxford, UK, 2011). (10.1093/acprof:oso/9780199692590.001.0001) / The Origins of Evolutionary Innovations: A Theory of Transformative Change in Living Systems by Wagner A (2011)
  44. D Corsaro, , Microsporidia-like parasites of amoebae belong to the early fungal lineage Rozellomycota. Parasitol Res 113, 1909–1918 (2014). (10.1007/s00436-014-3838-4) / Parasitol Res / Microsporidia-like parasites of amoebae belong to the early fungal lineage Rozellomycota by Corsaro D (2014)
  45. TY James, ML Berbee, No jacket required—new fungal lineage defies dress code: Recently described zoosporic fungi lack a cell wall during trophic phase. BioEssays 34, 94–102 (2012). (10.1002/bies.201100110) / BioEssays / No jacket required—new fungal lineage defies dress code: Recently described zoosporic fungi lack a cell wall during trophic phase by James TY (2012)
  46. YY Sokolova, GG Paskerova, YM Rotari, ES Nassonova, AV Smirnov, Fine structure of Metchnikovella incurvata Caullery and Mesnil 1914 (microsporidia), a hyperparasite of gregarines Polyrhabdina sp. from the polychaete Pygospio elegans. Parasitology 140, 855–867 (2013). (10.1017/S0031182013000036) / Parasitology / Fine structure of Metchnikovella incurvata Caullery and Mesnil 1914 (microsporidia), a hyperparasite of gregarines Polyrhabdina sp. from the polychaete Pygospio elegans by Sokolova YY (2013)
  47. A Stamatakis, RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690 (2006). (10.1093/bioinformatics/btl446) / Bioinformatics / RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models by Stamatakis A (2006)
Dates
Type When
Created 10 years, 10 months ago (Oct. 14, 2014, midnight)
Deposited 3 years, 2 months ago (June 7, 2022, 7:50 a.m.)
Indexed 4 weeks ago (Aug. 6, 2025, 8:01 a.m.)
Issued 10 years, 10 months ago (Oct. 13, 2014)
Published 10 years, 10 months ago (Oct. 13, 2014)
Published Online 10 years, 10 months ago (Oct. 13, 2014)
Published Print 10 years, 10 months ago (Oct. 28, 2014)
Funders 0

None

@article{Haag_2014, title={Evolution of a morphological novelty occurred before genome compaction in a lineage of extreme parasites}, volume={111}, ISSN={1091-6490}, url={http://dx.doi.org/10.1073/pnas.1410442111}, DOI={10.1073/pnas.1410442111}, number={43}, journal={Proceedings of the National Academy of Sciences}, publisher={Proceedings of the National Academy of Sciences}, 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}, year={2014}, month=oct, pages={15480–15485} }