1932

Abstract

Microsporidia are eukaryotic parasites of many animals that appear to have adapted to an obligate intracellular lifestyle by modifying the morphology and content of their cells. Living inside other cells, they have lost many, or all, metabolic functions, resulting in genomes that are always gene poor and often very small. The minute content of microsporidian genomes led many to assume that these parasites are biochemically static and uninteresting. However, recent studies have demonstrated that these organisms can be surprisingly complex and dynamic. In this review I detail the most significant recent advances in microsporidian genomics and discuss how these have affected our understanding of many biological aspects of these peculiar eukaryotic intracellular pathogens.

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2015-10-15
2024-03-28
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Literature Cited

  1. Akiyoshi DE, Morrison HG, Lei S, Feng X, Zhang Q. 1.  et al. 2009. Genomic survey of the non-cultivatable opportunistic human pathogen, Enterocytozoon bieneusi. PLOS Pathog. 5:e1000261 [Google Scholar]
  2. Bakowski MA, Desjardins CA, Smelkinson MG, Dunbar TA, Lopez-Moyado IF. 2.  et al. 2014. Ubiquitin-mediated response to microsporidia and virus infection in C. elegans. PLOS Pathog. 10:e1004200 [Google Scholar]
  3. Balla KM, Troemel ER. 3.  2013. Caenorhabditis elegans as a model for intracellular pathogen infection. Cell. Microbiol. 15:1313–22 [Google Scholar]
  4. Barlow LD, Dacks JB, Wideman JG. 4.  2014. From all to (nearly) none: tracing adaptin evolution in fungi. Cell. Logist. 4:e28114 [Google Scholar]
  5. Becnel JJ, Andreadis TG. 5.  1999. Microsporidia in insects. The Microsporidia and Microsporidiosis WLM Wittner, LM Weiss 447–501 Washington, DC: Am. Soc. Microbiol. [Google Scholar]
  6. Campbell SE, Williams TA, Yousuf A, Soanes DM, Paszkiewicz KH, Williams BA. 6.  2013. The genome of Spraguea lophii and the basis of host-microsporidian interactions. PLOS Genet. 9:e1003676 [Google Scholar]
  7. Capella-Gutierrez S, Marcet-Houben M, Gabaldon T. 7.  2012. Phylogenomics supports microsporidia as the earliest diverging clade of sequenced fungi. BMC Biol. 10:47 [Google Scholar]
  8. Cavalier-Smith T. 8.  1987. Eukaryotes with no mitochondria. Nature 326:332–33 [Google Scholar]
  9. Cornman RS, Chen YP, Schatz MC, Street C, Zhao Y. 9.  et al. 2009. Genomic analyses of the microsporidian Nosema ceranae, an emergent pathogen of honey bees. PLOS Pathog. 5:e1000466 [Google Scholar]
  10. Corradi N, Burri L, Keeling PJ. 10.  2008. mRNA processing in Antonospora locustae spores. Mol. Genet. Genomics 280:565–74 [Google Scholar]
  11. Corradi N, Gangaeva A, Keeling PJ. 11.  2008. Comparative profiling of overlapping transcription in the compacted genomes of microsporidia Antonospora locustae and Encephalitozoon cuniculi. Genomics 91:388–93 [Google Scholar]
  12. Corradi N, Haag KL, Pombert JF, Ebert D, Keeling PJ. 12.  2009. Draft genome sequence of the Daphnia pathogen Octosporea bayeri: insights into the gene content of a large microsporidian genome and a model for host-parasite interactions. Genome Biol. 10:R106 [Google Scholar]
  13. Corradi N, Keeling P. 13.  2009. Microsporidia: a journey through radical taxonomical revisions. Fungal Biol. Rev. 23:1–8 [Google Scholar]
  14. Corradi N, Pombert JF, Farinelli L, Didier ES, Keeling PJ. 14.  2010. The complete sequence of the smallest known nuclear genome from the microsporidian Encephalitozoon intestinalis. Nat. Commun. 1:77 [Google Scholar]
  15. Corradi N, Slamovits CH. 15.  2011. The intriguing nature of microsporidian genomes. Brief. Funct. Genomics 10:115–24 [Google Scholar]
  16. Corsaro D, Walochnik J, Venditti D, Steinmann J, Muller KD, Michel R. 16.  2014. Microsporidia-like parasites of amoebae belong to the early fungal lineage Rozellomycota. Parasitol. Res. 113:1909–18 [Google Scholar]
  17. Coyle CM, Weiss LM, Rhodes LV 3rd, Cali A, Takvorian PM. 17.  et al. 2004. Fatal myositis due to the microsporidian Brachiola algerae, a mosquito pathogen. N. Engl. J. Med. 351:42–47 [Google Scholar]
  18. Cuomo CA, Desjardins CA, Bakowski MA, Goldberg J, Ma AT. 18.  et al. 2012. Microsporidian genome analysis reveals evolutionary strategies for obligate intracellular growth. Genome Res. 22:2478–88 [Google Scholar]
  19. Didier ES, Weiss LM. 19.  2011. Microsporidiosis: not just in AIDS patients. Curr. Opin. Infect. Dis. 24:490–95 [Google Scholar]
  20. Ene IV, Bennett RJ. 20.  2014. The cryptic sexual strategies of human fungal pathogens. Nat. Rev. 12:239–51 [Google Scholar]
  21. Estes KA, Szumowski SC, Troemel ER. 21.  2011. Non-lytic, actin-based exit of intracellular parasites from C. elegans intestinal cells. PLOS Pathog. 7:e1002227 [Google Scholar]
  22. Fast NM, Law JS, Williams BA, Keeling PJ. 22.  2003. Bacterial catalase in the microsporidian Nosema locustae: implications for microsporidian metabolism and genome evolution. Eukaryot. Cell 2:1069–75 [Google Scholar]
  23. Franzen C. 23.  2004. Microsporidia: How can they invade other cells?. Trends Parasitol. 20:275–79 [Google Scholar]
  24. Gill EE, Fast NM. 24.  2006. Assessing the microsporidia-fungi relationship: Combined phylogenetic analysis of eight genes. Gene 375:103–9 [Google Scholar]
  25. Gill EE, Fast NM. 25.  2007. Stripped-down DNA repair in a highly reduced parasite. BMC Mol. Biol. 8:24 [Google Scholar]
  26. Guo X, Gao J, Li F, Wang J. 26.  2014. Evidence of horizontal transfer of non-autonomous Lep1 Helitrons facilitated by host-parasite interactions. Sci. Rep. 4:5119 [Google Scholar]
  27. Haag KL, James TY, Pombert J-F, Larsson R, Schaer TMM. 27.  et al. Evolution of a morphological novelty occurred before genome compaction in a lineage of extreme parasites. PNAS 111:15480–85 [Google Scholar]
  28. Haag KL, Sheikh-Jabbari E, Ben-Ami F, Ebert D. 28.  2013. Microsatellite and single-nucleotide polymorphisms indicate recurrent transitions to asexuality in a microsporidian parasite. J. Evol. Biol. 26:1117–28 [Google Scholar]
  29. Haag KL, Traunecker E, Ebert D. 29.  2013. Single-nucleotide polymorphisms of two closely related microsporidian parasites suggest a clonal population expansion after the last glaciation. Mol. Ecol. 22:314–26 [Google Scholar]
  30. Heinz E, Williams TA, Nakjang S, Noel CJ, Swan DC. 30.  et al. 2012. The genome of the obligate intracellular parasite Trachipleistophora hominis: new insights into microsporidian genome dynamics and reductive evolution. PLOS Pathog. 8:e1002979 [Google Scholar]
  31. Heitman J. 31.  2010. Evolution of eukaryotic microbial pathogens via covert sexual reproduction. Cell Host Microbe 8:86–99 [Google Scholar]
  32. Heitman J, Sun S, James TY. 32.  2012. Evolution of fungal sexual reproduction. Mycologia 105:1–27 [Google Scholar]
  33. Higes M, Martin-Hernandez R, Botias C, Bailon EG, Gonzalez-Porto AV. 33.  et al. 2008. How natural infection by Nosema ceranae causes honeybee colony collapse. Environ. Microbiol. 10:2659–69 [Google Scholar]
  34. Hirt RP, Healy B, Vossbrinck CR, Canning EU, Embley TM. 34.  1997. A mitochondrial Hsp70 orthologue in Vairimorpha necatrix: molecular evidence that microsporidia once contained mitochondria. Curr. Biol. 7:995–98 [Google Scholar]
  35. Hirt RP, Logsdon JM Jr, Healy B, Dorey MW, Doolittle WF, Embley TM. 35.  1999. Microsporidia are related to Fungi: evidence from the largest subunit of RNA polymerase II and other proteins. PNAS 96:580–85 [Google Scholar]
  36. Ironside JE. 36.  2013. Diversity and recombination of dispersed ribosomal DNA and protein coding genes in microsporidia. PLOS ONE 8:e55878 [Google Scholar]
  37. Ishihara R. 37.  1969. The life cycle of Nosema bombycis as revealed in tissue culture cells of Bombyx mori. J. Invertebr. Pathol. 14:316–20 [Google Scholar]
  38. James TY, Kauff F, Schoch CL, Matheny PB, Hofstetter V. 38.  et al. 2006. Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature 443:818–22 [Google Scholar]
  39. James TY, Pelin A, Bonen L, Ahrendt S, Sain D. 39.  et al. 2013. Shared signatures of parasitism and phylogenomics unite Cryptomycota and microsporidia. Curr. Biol. 23:1548–53 [Google Scholar]
  40. Jones MD, Forn I, Gadelha C, Egan MJ, Bass D. 40.  et al. 2011. Discovery of novel intermediate forms redefines the fungal tree of life. Nature 474:200–3 [Google Scholar]
  41. Karpov SA, Mamkaeva MA, Aleoshin VV, Nassonova E, Lilje O, Gleason FH. 41.  2014. Morphology, phylogeny, and ecology of the aphelids (Aphelidea, Opisthokonta) and proposal for the new superphylum Opisthosporidia. Front. Microbiol. 5:112 [Google Scholar]
  42. Karpov SA, Mamkaeva MA, Benzerara K, Moreira D, Lopez-Garcia P. 42.  2014. Molecular phylogeny and ultrastructure of Aphelidium aff. melosirae (Aphelida, Opisthosporidia). Protist 165:512–26 [Google Scholar]
  43. Katinka MD, Duprat S, Cornillot E, Metenier G, Thomarat F. 43.  et al. 2001. Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature 414:450–53 [Google Scholar]
  44. Keeling PJ, Corradi N. 44.  2011. Shrink it or lose it: balancing loss of function with shrinking genomes in the microsporidia. Virulence 2:67–70 [Google Scholar]
  45. Keeling PJ, Corradi N, Morrison HG, Haag KL, Ebert D. 45.  et al. 2010. The reduced genome of the parasitic microsporidian Enterocytozoon bieneusi lacks genes for core carbon metabolism. Genome Biol. Evol. 2:304–9 [Google Scholar]
  46. Keeling PJ, Doolittle WF. 46.  1996. Alpha-tubulin from early-diverging eukaryotic lineages and the evolution of the tubulin family. Mol. Biol. Evol. 13:1297–305 [Google Scholar]
  47. Keeling PJ, Fast NM. 47.  2002. Microsporidia: biology and evolution of highly reduced intracellular parasites. Annu. Rev. Microbiol. 56:93–116 [Google Scholar]
  48. Keeling PJ, Luker MA, Palmer JD. 48.  2000. Evidence from beta-tubulin phylogeny that microsporidia evolved from within the fungi. Mol. Biol. Evol. 17:23–31 [Google Scholar]
  49. Keeling PJ, McFadden GI. 49.  1998. Origins of microsporidia. Trends Microbiol. 6:19–23 [Google Scholar]
  50. Kelly A, Dunn AM, Hatcher MJ. 50.  2002. Incomplete feminisation by the microsporidian sex ratio distorter, Nosema granulosis, and reduced transmission and feminisation efficiency at low temperatures. Int. J. Parasitol. 32:825–31 [Google Scholar]
  51. Krebes L, Zeidler L, Frankowski J, Bastrop R. 51.  2014. (Cryptic) sex in the microsporidian Nosema granulosis—evidence from parasite rDNA and host mitochondrial DNA. Infect. Genet. Evol. 21:259–68 [Google Scholar]
  52. Lartillot N, Lepage T, Blanquart S. 52.  2009. PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating. Bioinformatics 25:2286–88 [Google Scholar]
  53. Lee SC, Corradi N, Byrnes EJ 3rd, Torres-Martinez S, Dietrich FS. 53.  et al. 2008. Microsporidia evolved from ancestral sexual fungi. Curr. Biol. 18:1675–79 [Google Scholar]
  54. Lee SC, Corradi N, Doan S, Dietrich FS, Keeling PJ, Heitman J. 54.  2010. Evolution of the sex-related locus and genomic features shared in microsporidia and fungi. PLOS ONE 5:e10539 [Google Scholar]
  55. Lee SC, Heitman J. 55.  2014. Sex and the microsporidia. Microsporidia: Pathogens of Opportunity LM Weiss, JJ Becnel 231–244 Oxford, UK: Wiley [Google Scholar]
  56. Lee SC, Weiss LM, Heitman J. 56.  2009. Generation of genetic diversity in microsporidia via sexual reproduction and horizontal gene transfer. Commun. Integr. Biol. 2:414–17 [Google Scholar]
  57. Letcher PM, Lopez S, Schmieder R, Lee PA, Behnke C. 57.  et al. 2013. Characterization of Amoeboaphelidium protococcarum, an algal parasite new to the cryptomycota isolated from an outdoor algal pond used for the production of biofuel. PLOS ONE 8:e56232 [Google Scholar]
  58. Ma Z, Li C, Pan G, Li Z, Han B. 58.  et al. 2013. Genome-wide transcriptional response of silkworm (Bombyx mori) to infection by the microsporidian Nosema bombycis. PLOS ONE 8:e84137 [Google Scholar]
  59. 59. Microsporidia Comp. Seq. Proj. Consort 2010. Microsporidia comparative database Broad Inst. MIT Harv., Cambridge, MA. http://www.broadinstitute.org/annotation/genome/microsporidia_comparative/MultiHome.html
  60. Nakjang S, Williams TA, Heinz E, Watson AK, Foster PG. 60.  et al. 2013. Reduction and expansion in microsporidian genome evolution: new insights from comparative genomics. Genome Biol. Evol. 5:2285–303 [Google Scholar]
  61. Paldi N, Glick E, Oliva M, Zilberberg Y, Aubin L. 61.  et al. 2010. Effective gene silencing in a microsporidian parasite associated with honeybee (Apis mellifera) colony declines. Appl. Environ. Microbiol. 76:5960–64 [Google Scholar]
  62. Pan G, Xu J, Li T, Xia Q, Liu SL. 62.  et al. 2013. Comparative genomics of parasitic silkworm microsporidia reveal an association between genome expansion and host adaptation. BMC Genomics 14:186 [Google Scholar]
  63. Parisot N, Pelin A, Gasc C, Polonais V, Belkorchia A. 63.  et al. 2014. Microsporidian genomes harbor a diverse array of transposable elements that demonstrate an ancestry of horizontal exchange with metazoans. Genome Biol. Evol. 6:2289–300 [Google Scholar]
  64. Pelin A, Selman M, Aris-Brosou S, Farinelli L, Corradi N. 64.  2015. Genome analyses suggest the presence of polyploidy and recent human-driven expansions in eight global populations of the honeybee pathogen Nosema ceranae. Environ. Microbiol In press. doi: 10.1111/1462-2920.12883
  65. Peyretaillade E, Boucher D, Parisot N, Gasc C, Butler R. 65.  et al. 2014. Exploiting the architecture and the features of the microsporidian genomes to investigate diversity and impact of these parasites on ecosystems. Heredity 114:441–44 [Google Scholar]
  66. Peyretaillade E, El Alaoui H, Diogon M, Polonais V, Parisot N. 66.  et al. 2011. Extreme reduction and compaction of microsporidian genomes. Res. Microbiol. 162:598–606 [Google Scholar]
  67. Peyretaillade E, Goncalves O, Terrat S, Dugat-Bony E, Wincker P. 67.  et al. 2009. Identification of transcriptional signals in Encephalitozoon cuniculi widespread among Microsporidia phylum: support for accurate structural genome annotation. BMC Genomics 10:607 [Google Scholar]
  68. Peyretaillade E, Parisot N, Polonais V, Terrat S, Denonfoux J. 68.  et al. 2012. Annotation of microsporidian genomes using transcriptional signals. Nat. Commun. 3:1137 [Google Scholar]
  69. Pombert JF, Haag KL, Beidas S, Ebert D, Keeling PJ. 69.  2015. The Ordospora colligata genome: evolution of extreme reduction in Microsporidia and host-to-parasite horizontal gene transfer. mBio 6:e02400–14 [Google Scholar]
  70. Pombert JF, Selman M, Burki F, Bardell FT, Farinelli L. 70.  et al. 2012. Gain and loss of multiple functionally related, horizontally transferred genes in the reduced genomes of two microsporidian parasites. PNAS 109:12638–43 [Google Scholar]
  71. Richards TA, Hirt RP, Williams BA, Embley TM. 71.  2003. Horizontal gene transfer and the evolution of parasitic protozoa. Protist 154:17–32 [Google Scholar]
  72. Roger AJ, Svard SG, Tovar J, Clark CG, Smith MW. 72.  et al. 1998. A mitochondrial-like chaperonin 60 gene in Giardia lamblia: evidence that diplomonads once harbored an endosymbiont related to the progenitor of mitochondria. PNAS 95:229–34 [Google Scholar]
  73. Roth O, Ebert D, Vizoso DB, Bieger A, Lass S. 73.  2008. Male-biased sex-ratio distortion caused by Octosporea bayeri, a vertically and horizontally-transmitted parasite of Daphnia magna. Int. J. Parasitol. 38:969–79 [Google Scholar]
  74. Sagastume S, del Aguila C, Martin-Hernandez R, Higes M, Henriques-Gil N. 74.  2011. Polymorphism and recombination for rDNA in the putatively asexual microsporidian Nosema ceranae, a pathogen of honeybees. Environ. Microbiol. 13:84–95 [Google Scholar]
  75. Sapir A, Dillman AR, Connon SA, Grupe BM, Ingels J. 75.  et al. 2014. Microsporidia-nematode associations in methane seeps reveal basal fungal parasitism in the deep sea. Front. Microbiol. 5:43 [Google Scholar]
  76. Selman M, Corradi N. 76.  2011. Microsporidia: horizontal gene transfers in vicious parasites. Mobile Genet. Elem. 1:251–55 [Google Scholar]
  77. Selman M, Pombert JF, Solter L, Farinelli L, Weiss LM. 77.  et al. 2011. Acquisition of an animal gene by microsporidian intracellular parasites. Curr. Biol. 21:R576–77 [Google Scholar]
  78. Selman M, Sak B, Kvac M, Farinelli L, Weiss LM, Corradi N. 78.  2013. Extremely reduced levels of heterozygosity in the vertebrate pathogen Encephalitozoon cuniculi. Eukaryot. Cell 12:496–502 [Google Scholar]
  79. Senderskiy IV, Timofeev SA, Seliverstova EV, Pavlova OA, Dolgikh VV. 79.  2014. Secretion of Antonospora (Paranosema) locustae proteins into infected cells suggests an active role of microsporidia in the control of host programs and metabolic processes. PLOS ONE 9:e93585 [Google Scholar]
  80. Shiflett AM, Johnson PJ. 80.  2010. Mitochondrion-related organelles in eukaryotic protists. Annu. Rev. Microbiol. 64:409–29 [Google Scholar]
  81. Simakova AV, Vossbrinck CR, Andreadis TG. 81.  2008. Molecular and ultrastructural characterization of Andreanna caspii n. gen., n. sp. (Microsporida: Amblyosporidae), a parasite of Ochlerotatus caspius (Diptera: Culicidae). J. Invertebr. Pathol 99:302–11 [Google Scholar]
  82. Slamovits CH, Fast NM, Law JS, Keeling PJ. 82.  2004. Genome compaction and stability in microsporidian intracellular parasites. Curr. Biol. 14:891–96 [Google Scholar]
  83. Slamovits CH, Keeling PJ. 83.  2004. Class II photolyase in a microsporidian intracellular parasite. J. Mol. Biol. 341:713–21 [Google Scholar]
  84. Sokolova YY, Fuxa JR. 84.  2008. Biology and life-cycle of the microsporidium Kneallhazia solenopsae Knell Allan Hazard 1977 gen. n., comb. n., from the fire ant Solenopsis invicta. Parasitology 135:903–29 [Google Scholar]
  85. Sokolova YY, Pelin A, Hawke J, Corradi N. 85.  2015. Morphology and phylogeny of Agmasoma penaei (Microsporidia) from the type host, Litopenaeus setiferus, and the type locality, Louisiana, USA. Int. J. Parasitol 45:1–16 [Google Scholar]
  86. Stentiford GD, Feist SW, Stone DM, Bateman KS, Dunn AM. 86.  2013. Microsporidia: diverse, dynamic, and emergent pathogens in aquatic systems. Trends Parasitol. 29:567–78 [Google Scholar]
  87. Szumowski SC, Botts MR, Popovich JJ, Smelkinson MG, Troemel ER. 87.  2014. The small GTPase RAB-11 directs polarized exocytosis of the intracellular pathogen N. parisii for fecal-oral transmission from C. elegans.. PNAS 111:8215–20 [Google Scholar]
  88. Szumowski SC, Estes KA, Troemel ER. 88.  2012. Preparing a discreet escape: Microsporidia reorganize host cytoskeleton prior to non-lytic exit from C. elegans intestinal cells. Worm 1:207–11 [Google Scholar]
  89. Troemel ER, Felix MA, Whiteman NK, Barriere A, Ausubel FM. 89.  2008. Microsporidia are natural intracellular parasites of the nematode Caenorhabditis elegans. PLOS Biol. 6:2736–52 [Google Scholar]
  90. Tsaousis AD, Kunji ER, Goldberg AV, Lucocq JM, Hirt RP, Embley TM. 90.  2008. A novel route for ATP acquisition by the remnant mitochondria of Encephalitozoon cuniculi. Nature 453:553–56 [Google Scholar]
  91. Vávra J, Kamler M, Modrý D, Koudela B. 91.  2011. Opportunistic nature of the mammalian microsporidia: experimental transmission of Trachipleistophora extenrec (Fungi: Microsporidia) between mammalian and insect hosts. Parasitol. Res. 108:1565–73 [Google Scholar]
  92. Vávra J, Larsson JIR. 92.  1999. Structure of the microsporidia. The Microsporidia and Microsporidiosis M Wittner, LM Weiss 7–84 Washington, DC: Am. Soc. Microbiol. [Google Scholar]
  93. Vávra J, Lukes J. 93.  2013. Microsporidia and ‘the art of living together’. Adv. Parasitol. 82:253–319 [Google Scholar]
  94. Williams BA, Haferkamp I, Keeling PJ. 94.  2008. An ADP/ATP-specific mitochondrial carrier protein in the microsporidian Antonospora locustae. J. Mol. Biol. 375:1249–57 [Google Scholar]
  95. Williams BA, Hirt RP, Lucocq JM, Embley TM. 95.  2002. A mitochondrial remnant in the microsporidian Trachipleistophora hominis. Nature 418:865–96 [Google Scholar]
  96. Williams BA, Slamovits CH, Patron NJ, Fast NM, Keeling PJ. 96.  2005. A high frequency of overlapping gene expression in compacted eukaryotic genomes. PNAS 102:10936–41 [Google Scholar]
  97. Xiang H, Pan G, Vossbrinck CR, Zhang R, Xu J. 97.  et al. 2010. A tandem duplication of manganese superoxide dismutase in Nosema bombycis and its evolutionary origins. J. Mol. Evol. 71:401–14 [Google Scholar]
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