Evolution of microsporidia: An extremely successful group of eukaryotic intracellular parasites

1. Han B, Weiss LM. Microsporidia: Obligate Intracellular Pathogens Within the Fungal Kingdom. Microbiol Spectr. 2017;5. doi: 10.1128/microbiolspec.FUNK-0018-2016 28944750

2. Cuomo CA, Desjardins CA, Bakowski MA, Goldberg J, Ma AT, Becnel JJ, et al. Microsporidian genome analysis reveals evolutionary strategies for obligate intracellular growth. Genome Res. 2012;22: 2478–2488. doi: 10.1101/gr.142802.112 22813931

3. Desjardins CA, Sanscrainte ND, Goldberg JM, Heiman D, Young S, Zeng Q, et al. Contrasting host-pathogen interactions and genome evolution in two generalist and specialist microsporidian pathogens of mosquitoes. Nat Commun. 2015;6: 7121. doi: 10.1038/ncomms8121 25968466

4. Ndikumana S, Pelin A, Williot A, Sanders JL, Kent M, Corradi N. Genome Analysis of Pseudoloma neurophilia: A Microsporidian Parasite of Zebrafish (Danio rerio). J Eukaryot Microbiol. 2017;64: 18–30. doi: 10.1111/jeu.12331 27230544

5. Selman M, Sak B, Kvac M, Farinelli L, Weiss LM, Corradi N. Extremely reduced levels of heterozygosity in the vertebrate pathogen Encephalitozoon cuniculi. Eukaryot Cell. 2013;12: 496–502. doi: 10.1128/EC.00307-12 23376943

6. Nakjang S, Williams TA, Heinz E, Watson AK, Foster PG, Sendra KM, et al. Reduction and expansion in microsporidian genome evolution: new insights from comparative genomics. Genome Biol Evol. 2013;5: 2285–2303. doi: 10.1093/gbe/evt184 24259309

7. Keeling PJ, Fast NM. Microsporidia: biology and evolution of highly reduced intracellular parasites. Annu Rev Microbiol. 2002;56: 93–116. doi: 10.1146/annurev.micro.56.012302.160854 12142484

8. Galindo LJ, Torruella G, Moreira D, Timpano H, Paskerova G, Smirnov A, et al. Evolutionary Genomics of Metchnikovella incurvata (Metchnikovellidae): An Early Branching Microsporidium. Genome Biol Evol. 2018;10: 2736–2748. doi: 10.1093/gbe/evy205 30239727

9. Mikhailov KV, Simdyanov TG, Aleoshin VV. Genomic Survey of a Hyperparasitic Microsporidian Amphiamblys sp. (Metchnikovellidae). Genome Biol Evol. 2017;9: 454–467. doi: 10.1093/gbe/evw235 27694476

10. Shertz CA, Bastidas RJ, Li W, Heitman J, Cardenas ME. Conservation, duplication, and loss of the Tor signaling pathway in the fungal kingdom. BMC Genomics. 2010;11: 510. doi: 10.1186/1471-2164-11-510 20863387

11. Katinka MD, Duprat S, Cornillot E, Metenier G, Thomarat F, Prensier G, et al. Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature. 2001;414: 450–453. doi: 10.1038/35106579 11719806

12. Melnikov SV, Rivera KD, Ostapenko D, Makarenko A, Sanscrainte ND, Becnel JJ, et al. Error-prone protein synthesis in parasites with the smallest eukaryotic genome. Proc Natl Acad Sci U S A. 2018;115: E6245–E6253. doi: 10.1073/pnas.1803208115 29915081

13. Melnikov SV, Manakongtreecheep K, Rivera KD, Makarenko A, Pappin DJ, Soll D. Muller’s Ratchet and Ribosome Degeneration in the Obligate Intracellular Parasites Microsporidia. Int J Mol Sci. 2018;19. doi: 10.3390/ijms19124125 30572624

14. Barandun J, Hunziker M, Vossbrinck CR, Klinge S. Evolutionary compaction and adaptation visualized by the structure of the dormant microsporidian ribosome. Nat Microbiol. 2019. doi: 10.1038/s41564-019-0514-6 31332387

15. Williams BAP, Hirt RP, Lucocq JM, Embley TM. A mitochondrial remnant in the microsporidian Trachipleistophora hominis. Nature. 2002;418: 865–869. doi: 10.1038/nature00949 12192407

16. Dean P, Sendra KM, Williams TA, Watson AK, Major P, Nakjang S, et al. Transporter gene acquisition and innovation in the evolution of Microsporidia intracellular parasites. Nat Commun. 2018;9: 1709. doi: 10.1038/s41467-018-03923-4 29703975

17. Corradi N, Pombert J-F, Farinelli L, Didier ES, Keeling PJ. The complete sequence of the smallest known nuclear genome from the microsporidian Encephalitozoon intestinalis. Nat Commun. 2010;1: 77. doi: 10.1038/ncomms1082 20865802

18. Pombert J-F, Xu J, Smith DR, Heiman D, Young S, Cuomo CA, et al. Complete genome sequences from three genetically distinct strains reveal high intraspecies genetic diversity in the microsporidian Encephalitozoon cuniculi. Eukaryot Cell. 2013;12: 503–511. doi: 10.1128/EC.00312-12 23291622

19. Reinke AW, Balla KM, Bennett EJ, Troemel ER. Identification of microsporidia host-exposed proteins reveals a repertoire of rapidly evolving proteins. Nat Commun. 2017;8: 14023. doi: 10.1038/ncomms14023 28067236

20. Williams TA, Nakjang S, Campbell SE, Freeman MA, Eydal M, Moore K, et al. A Recent Whole-Genome Duplication Divides Populations of a Globally Distributed Microsporidian. Mol Biol Evol. 2016;33: 2002–2015. doi: 10.1093/molbev/msw083 27189558

21. Whelan TA, Lee NT, Lee RCH, Fast NM. Microsporidian Introns Retained against a Background of Genome Reduction: Characterization of an Unusual Set of Introns. Genome Biol Evol. 2019;11: 263–269. doi: 10.1093/gbe/evy260 30496512

22. Huang Q. Evolution of Dicer and Argonaute orthologs in microsporidian parasites. Infect Genet Evol J Mol Epidemiol Evol Genet Infect Dis. 2018;65: 329–332. doi: 10.1016/j.meegid.2018.08.011 30142384

23. Wiredu Boakye D, Jaroenlak P, Prachumwat A, Williams TA, Bateman KS, Itsathitphaisarn O, et al. Decay of the glycolytic pathway and adaptation to intranuclear parasitism within Enterocytozoonidae microsporidia. Environ Microbiol. 2017;19: 2077–2089. doi: 10.1111/1462-2920.13734 28345194

24. Keeling P. Five questions about microsporidia. PLoS Pathog. 2009;5: e1000489. doi: 10.1371/journal.ppat.1000489 19779558

25. Jones MDM, Forn I, Gadelha C, Egan MJ, Bass D, Massana R, et al. Discovery of novel intermediate forms redefines the fungal tree of life. Nature. 2011;474: 200–203. doi: 10.1038/nature09984 21562490

26. James TY, Pelin A, Bonen L, Ahrendt S, Sain D, Corradi N, et al. Shared signatures of parasitism and phylogenomics unite Cryptomycota and microsporidia. Curr Biol CB. 2013;23: 1548–1553. doi: 10.1016/j.cub.2013.06.057 23932404

27. Quandt CA, Beaudet D, Corsaro D, Walochnik J, Michel R, Corradi N, et al. The genome of an intranuclear parasite, Paramicrosporidium saccamoebae, reveals alternative adaptations to obligate intracellular parasitism. eLife. 2017;6. doi: 10.7554/eLife.29594 29171834

28. Haag KL, James TY, Pombert J-F, Larsson R, Schaer TMM, Refardt D, et al. Evolution of a morphological novelty occurred before genome compaction in a lineage of extreme parasites. Proc Natl Acad Sci U S A. 2014;111: 15480–15485. doi: 10.1073/pnas.1410442111 25313038

29. Bass D, Czech L, Williams BAP, Berney C, Dunthorn M, Mahe F, et al. Clarifying the Relationships between Microsporidia and Cryptomycota. J Eukaryot Microbiol. 2018;65: 773–782. doi: 10.1111/jeu.12519 29603494

30. Corsaro D, Walochnik J, Venditti D, Steinmann J, Muller K-D, Michel R. Microsporidia-like parasites of amoebae belong to the early fungal lineage Rozellomycota. Parasitol Res. 2014;113: 1909–1918. doi: 10.1007/s00436-014-3838-4 24652444

31. Zhang G, Sachse M, Prevost M-C, Luallen RJ, Troemel ER, Felix M-A. A Large Collection of Novel Nematode-Infecting Microsporidia and Their Diverse Interactions with Caenorhabditis elegans and Other Related Nematodes. PLoS Pathog. 2016;12: e1006093. doi: 10.1371/journal.ppat.1006093 27942022

32. Shaw RW, Kent ML, Brown AM, Whipps CM, Adamson ML. Experimental and natural host specificity of Loma salmonae (Microsporidia). Dis Aquat Organ. 2000;40: 131–136. doi: 10.3354/dao040131 10782347

33. Solter LF, Pilarska DK, McManus ML, Zubrik M, Patocka J, Huang W-F, et al. Host specificity of microsporidia pathogenic to the gypsy moth, Lymantria dispar (L.): field studies in Slovakia. J Invertebr Pathol. 2010;105: 1–10. doi: 10.1016/j.jip.2010.04.009 20435042

34. Hinney B, Sak B, Joachim A, Kvac M. More than a rabbit’s tale—Encephalitozoon spp. in wild mammals and birds. Int J Parasitol Parasites Wildl. 2016;5: 76–87. doi: 10.1016/j.ijppaw.2016.01.001 28560162

35. Luallen RJ, Reinke AW, Tong L, Botts MR, Felix M-A, Troemel ER. Discovery of a Natural Microsporidian Pathogen with a Broad Tissue Tropism in Caenorhabditis elegans. PLoS Pathog. 2016;12: e1005724. doi: 10.1371/journal.ppat.1005724 27362540

36. Johny S, Larson TM, Solter LF, Edwards KA, Whitman DW. Phylogenetic characterization of Encephalitozoon romaleae (Microsporidia) from a grasshopper host: relationship to Encephalitozoon spp. infecting humans. Infect Genet Evol J Mol Epidemiol Evol Genet Infect Dis. 2009;9: 189–195. doi: 10.1016/j.meegid.2008.10.010 19027883

37. Stentiford GD, Bass D, Williams BAP. Ultimate opportunists-The emergent Enterocytozoon group Microsporidia. PLoS Pathog. 2019;15: e1007668. doi: 10.1371/journal.ppat.1007668 31048922

38. Watson AK, Williams TA, Williams BAP, Moore KA, Hirt RP, Embley TM. Transcriptomic profiling of host-parasite interactions in the microsporidian Trachipleistophora hominis. BMC Genomics. 2015;16: 983. doi: 10.1186/s12864-015-1989-z 26589282

39. Watts MR, Chan RCF, Cheong EYL, Brammah S, Clezy KR, Tong C, et al. Anncaliia algerae microsporidial myositis. Emerg Infect Dis. 2014;20: 185–191. doi: 10.3201/eid2002.131126 24447398

40. Vavra J, Lukes J. Microsporidia and “the art of living together”. Adv Parasitol. 2013;82: 253–319. doi: 10.1016/B978-0-12-407706-5.00004-6 23548087

41. Ardila-Garcia AM, Raghuram N, Sihota P, Fast NM. Microsporidian diversity in soil, sand, and compost of the Pacific Northwest. J Eukaryot Microbiol. 2013;60: 601–608. doi: 10.1111/jeu.12066 23869987

42. Williams BAP, Hamilton KM, Jones MD, Bass D. Group-specific environmental sequencing reveals high levels of ecological heterogeneity across the microsporidian radiation. Environ Microbiol Rep. 2018;10: 328–336. doi: 10.1111/1758-2229.12642 29578312

43. Larsen BB, Miller EC, Rhodes MK, Wiens JJ. Inordinate Fondness Multiplied and Redistributed: the Number of Species on Earth and the New Pie of Life. Q Rev Biol. 2017;92: 229–265. doi: 10.1086/693564

44. Huang Y, Zheng S, Mei X, Yu B, Sun B, Li B, et al. A secretory hexokinase plays an active role in the proliferation of Nosema bombycis. PeerJ. 2018;6: e5658. doi: 10.7717/peerj.5658 30258733

45. Ferguson S, Lucocq J. The invasive cell coat at the microsporidian Trachipleistophora hominis-host cell interface contains secreted hexokinases. MicrobiologyOpen. 2019;8: e00696. doi: 10.1002/mbo3.696 30051624

46. Senderskiy IV, Timofeev SA, Seliverstova EV, Pavlova OA, Dolgikh VV. 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. 2014;9: e93585. doi: 10.1371/journal.pone.0093585 24705470

47. Major P, Sendra KM, Dean P, Williams TA, Watson AK, Thwaites DT, et al. A new family of cell surface located purine transporters in Microsporidia and related fungal endoparasites. eLife. 2019;8. doi: 10.7554/eLife.47037 31355745

48. Han B, Ma Y, Tu V, Tomita T, Mayoral J, Williams T, et al. Microsporidia Interact with Host Cell Mitochondria via Voltage-Dependent Anion Channels Using Sporoplasm Surface Protein 1. mBio. 2019;10. doi: 10.1128/mBio.01944-19 31431557

49. Reinke AW, Troemel ER. The Development of Genetic Modification Techniques in Intracellular Parasites and Potential Applications to Microsporidia. PLoS Pathog. 2015;11: e1005283. doi: 10.1371/journal.ppat.1005283 26720003

50. Franchet A, Niehus S, Caravello G, Ferrandon D. Phosphatidic acid as a limiting host metabolite for the proliferation of the microsporidium Tubulinosema ratisbonensis in Drosophila flies. Nat Microbiol. 2019;4: 645–655. doi: 10.1038/s41564-018-0344-y 30692666