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Abstract

This review explores the origins of intracellular parasitism, an intriguing facet of symbiosis, where one organism harms its host, potentially becoming deadly. We focus on three distantly related groups of single-celled eukaryotes, namely Kinetoplastea, Holomycota, and Apicomplexa, which contain multiple species-rich lineages of intracellular parasites. Using comparative analysis of morphological, physiological, and molecular features of kinetoplastids, microsporidians, and sporozoans, as well as their closest free-living relatives, we reveal the evolutionary trajectories and adaptations that enabled the transition to intracellular parasitism. Intracellular parasites have evolved various efficient mechanisms for host acquisition and exploitation, allowing them to thrive in a variety of hosts. Each group has developed unique features related to the parasitic lifestyle, involving dedicated protein families associated with host cell invasion, survival, and exit. Indeed, parallel evolution has led to distinct lineages of intracellular parasites employing diverse traits and approaches to achieve similar outcomes.

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/content/journals/10.1146/annurev-micro-041222-025305
2024-11-20
2025-03-14
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Literature Cited

  1. 1.
    Adl SM, Bass D, Lane CE, Lukeš J, Schoch CL, et al. 2019.. Revisions to the classification, nomenclature, and diversity of eukaryotes. . J. Eukaryot. Microbiol. 66::4119
    [Crossref] [Google Scholar]
  2. 2.
    Albanaz ATS, Carrington M, Frolov AO, Ganyukova AI, Gerasimov ES, et al. 2023.. Shining the spotlight on the neglected: new high-quality genome assemblies as a gateway to understanding the evolution of Trypanosomatidae. . BMC Genom. 24::471
    [Crossref] [Google Scholar]
  3. 3.
    Albanaz ATS, Gerasimov ES, Shaw JJ, Sádlová J, Lukeš J, et al. 2021.. Genome analysis of Endotrypanum and Porcisia spp., closest phylogenetic relatives of Leishmania, highlights the role of amastins in shaping pathogenicity. . Genes 12::444
    [Crossref] [Google Scholar]
  4. 4.
    Alexander WG, Wisecaver JH, Rokas A, Hittinger CT. 2016.. Horizontally acquired genes in early-diverging pathogenic fungi enable the use of host nucleosides and nucleotides. . PNAS 113::411621
    [Crossref] [Google Scholar]
  5. 5.
    Arcila F, Meunier J. 2020.. Friend or foe? The apparent benefits of gregarine (Apicomplexa: Sporozoa) infection in the European earwig. . Int. J. Parasitol. 50::46169
    [Crossref] [Google Scholar]
  6. 6.
    Bartholomeu DC, de Paiva RM, Mendes TA, DaRocha WD, Teixeira SM. 2014.. Unveiling the intracellular survival gene kit of trypanosomatid parasites. . PLOS Pathog. 10::e1004399
    [Crossref] [Google Scholar]
  7. 7.
    Bartošová-Sojková P, Oppenheim RD, Soldati-Favre D, Lukeš J. 2015.. Epicellular apicomplexans: parasites “on the way in. .” PLOS Pathog. 11::e1005080
    [Crossref] [Google Scholar]
  8. 8.
    Bass D, Czech L, Williams BAP, Berney C, Dunthorn M, et al. 2018.. Clarifying the relationships between Microsporidia and Cryptomycota. . J. Eukaryot. Microbiol. 65::77382
    [Crossref] [Google Scholar]
  9. 9.
    Batista MF, Najera CA, Meneghelli I, Bahia D. 2020.. The parasitic intracellular lifestyle of trypanosomatids: parasitophorous vacuole development and survival. . Front. Cell Dev. Biol. 8::396
    [Crossref] [Google Scholar]
  10. 10.
    Buchanan KL, Murphy JW. 1998.. What makes Cryptococcus neoformans a pathogen?. Emerg. Infect. Dis. 4::7183
    [Crossref] [Google Scholar]
  11. 11.
    Burrell A, Tomley FM, Vaughan S, Marugan-Hernandez V. 2020.. Life cycle stages, specific organelles and invasion mechanisms of Eimeria species. . Parasitology 147::26378
    [Crossref] [Google Scholar]
  12. 12.
    Butenko A, Hammond M, Field MC, Ginger ML, Yurchenko V, Lukeš J. 2021.. Reductionist pathways for parasitism in euglenozoans? Expanded datasets provide new insights. . Trends Parasitol. 37::10016
    [Crossref] [Google Scholar]
  13. 13.
    Cao L, Peng B, Yao L, Zhang X, Sun K, et al. 2010.. The ancient function of RB-E2F pathway: insights from its evolutionary history. . Biol. Direct 5::55
    [Crossref] [Google Scholar]
  14. 14.
    Capewell P, Cooper A, Clucas C, Weir W, MacLeod A. 2015.. A co-evolutionary arms race: trypanosomes shaping the human genome, humans shaping the trypanosome genome. . Parasitology 142:(Suppl. 1):S10819
    [Crossref] [Google Scholar]
  15. 15.
    Carlson CJ, Dallas TA, Alexander LW, Phelan AL, Phillips AJ. 2020.. What would it take to describe the global diversity of parasites?. Proc. Biol. Sci. 287::20201841
    [Google Scholar]
  16. 16.
    Casadevall A. 2008.. Evolution of intracellular pathogens. . Annu. Rev. Microbiol. 62::1933
    [Crossref] [Google Scholar]
  17. 17.
    Castillo JC, Ferreira ABB, Trisnadi N, Barillas-Mury C. 2017.. Activation of mosquito complement antiplasmodial response requires cellular immunity. . Sci. Immunol. 2::eaal1505
    [Crossref] [Google Scholar]
  18. 18.
    Cavalier-Smith T. 1993.. Kingdom Protozoa and its 18 phyla. . Microbiol. Rev. 57::95394
    [Crossref] [Google Scholar]
  19. 19.
    Cavalier-Smith T. 2018.. Kingdom Chromista and its eight phyla: a new synthesis emphasising periplastid protein targeting, cytoskeletal and periplastid evolution, and ancient divergences. . Protoplasma 255::297357
    [Crossref] [Google Scholar]
  20. 20.
    Chacón-Vargas K, McCarthy CO, Choi D, Wang L, Yu JH, Gibbons JGG. 2021.. Comparison of two Aspergillus oryzae genomes from different clades reveals independent evolution of alpha-amylase duplication, variation in secondary metabolism genes, and differences in primary metabolism. . Front. Microbiol. 12::691296
    [Crossref] [Google Scholar]
  21. 21.
    Coakley G, Maizels RM, Buck AH. 2015.. Exosomes and other extracellular vesicles: the new communicators in parasite infections. . Trends Parasitol. 31::47789
    [Crossref] [Google Scholar]
  22. 22.
    Corradi N, Slamovits CH. 2011.. The intriguing nature of microsporidian genomes. . Brief. Funct. Genom. 10::11524
    [Crossref] [Google Scholar]
  23. 23.
    Corsaro D. 2022.. Insights into Microsporidia evolution from early diverging Microsporidia. . In Microsporidia, Vol. 114, ed. LM Weiss, AW Reinke , pp. 7190. Cham, Switz:.: Springer
    [Google Scholar]
  24. 24.
    Corsaro D, Walochnik J, Venditti D, Hauroeder B, Michel R. 2020.. Solving an old enigma: Morellospora saccamoebae gen. nov., sp. nov. (Rozellomycota), a Sphaerita-like parasite of free-living amoebae. . Parasitol. Res. 119::92534
    [Crossref] [Google Scholar]
  25. 25.
    Corsaro D, Walochnik J, Venditti D, Steinmann J, Müller K-D, Michel R. 2014.. Microsporidia-like parasites of amoebae belong to the early fungal lineage Rozellomycota. . Parasitol. Res. 113::190918
    [Crossref] [Google Scholar]
  26. 26.
    Corsaro D, Wylezich C, Venditti D, Michel R, Walochnik J, Wegensteiner R. 2019.. Filling gaps in the microsporidian tree: rDNA phylogeny of Chytridiopsis typographi (Microsporidia: Chytridiopsida). . Parasitol. Res. 118::16980
    [Crossref] [Google Scholar]
  27. 27.
    Cova MM, Lamarque MH, Lebrun M. 2022.. How Apicomplexa parasites secrete and build their invasion machinery. . Annu. Rev. Microbiol. 76::61940
    [Crossref] [Google Scholar]
  28. 28.
    Cumbo VR, Baird AH, Moore RB, Negri AP, Neilan BA, et al. 2013.. Chromera velia is endosymbiotic in larvae of the reef corals Acropora digitifera and A. tenuis. . Protist 164::23744
    [Crossref] [Google Scholar]
  29. 29.
    Cuomo CA, Desjardins CA, Bakowski MA, Goldberg J, Ma AT, et al. 2012.. Microsporidian genome analysis reveals evolutionary strategies for obligate intracellular growth. . Genome Res. 22::247888
    [Crossref] [Google Scholar]
  30. 30.
    David V, Flegontov P, Gerasimov E, Tanifuji G, Hashimi H, et al. 2015.. Gene loss and error-prone RNA editing in the mitochondrion of Perkinsela, an endosymbiotic kinetoplastid. . mBio 6::e01498-15
    [Google Scholar]
  31. 31.
    de Castro Neto AL, da Silveira JF, Mortara RA. 2021.. Comparative analysis of virulence mechanisms of trypanosomatids pathogenic to humans. . Front. Cell. Infect. Microbiol. 11::669079
    [Crossref] [Google Scholar]
  32. 32.
    De Rycker M, Wyllie S, Horn D, Read KD, Gilbert IH. 2023.. Anti-trypanosomatid drug discovery: progress and challenges. . Nat. Rev. Microbiol. 21::3550
    [Crossref] [Google Scholar]
  33. 33.
    Dean P, Sendra KM, Williams TA, Watson AK, Major P, et al. 2018.. Transporter gene acquisition and innovation in the evolution of Microsporidia intracellular parasites. . Nat. Commun. 9::1709
    [Crossref] [Google Scholar]
  34. 34.
    Dyková I, Fiala I, Lom J, Lukeš J. 2003.. Perkinsiella amoebae-like endosymbionts of Neoparamoeba spp., relatives of the kinetoplastid Ichthyobodo. . Eur. J. Protistol. 39::3752
    [Crossref] [Google Scholar]
  35. 35.
    Dyková I, Veverková M, Fiala I, Macháčková B, Pecková H. 2003.. Nuclearia pattersoni sp n. (Filosea), a new species of amphizoic amoeba isolated from gills of roach (Rutilus rutilus), and its rickettsial endosymbiont. . Folia Parasitol. 50::16170
    [Crossref] [Google Scholar]
  36. 36.
    Etheridge RD. 2022.. Protozoan phagotrophy from predators to parasites: an overview of the enigmatic cytostome-cytopharynx complex of Trypanosoma cruzi. . J. Eukaryot. Microbiol. 69::e12896
    [Crossref] [Google Scholar]
  37. 37.
    Flegontova O, Flegontov P, Londoño PAC, Walczowski W, Šantić D, et al. 2020.. Environmental determinants of the distribution of planktonic diplonemids and kinetoplastids in the oceans. . Environ. Microbiol. 22::401431
    [Crossref] [Google Scholar]
  38. 38.
    Fokin SI, Schrallhammer M, Chiellini C, Verni F, Petroni G. 2014.. Free-living ciliates as potential reservoirs for eukaryotic parasites: occurrence of a trypanosomatid in the macronucleus of Euplotes encysticus. . Parasites Vectors 7::203
    [Crossref] [Google Scholar]
  39. 39.
    Füssy Z, Masařová P, Kručinská J, Esson HJ, Oborník M. 2017.. Budding of the alveolate alga Vitrella brassicaformis resembles sexual and asexual processes in apicomplexan parasites. . Protist 168::8091
    [Crossref] [Google Scholar]
  40. 40.
    Gabaldón T, Völcker E, Torruella G. 2022.. On the biology, diversity and evolution of nucleariid amoebae (Amorphea, Obazoa, Opisthokonta). . Protist 173::25895
    [Crossref] [Google Scholar]
  41. 41.
    Galindo LJ, López-García P, Torruella G, Karpov S, Moreira D. 2021.. Phylogenomics of a new fungal phylum reveals multiple waves of reductive evolution across Holomycota. . Nat. Commun. 12::4973
    [Crossref] [Google Scholar]
  42. 42.
    Galindo LJ, Torruella G, López-García P, Ciobanu M, Gutiérrez-Preciado A, et al. 2022.. Phylogenomics supports the monophyly of aphelids and fungi and identifies new molecular synapomorphies. . Syst. Biol. 72::50515
    [Crossref] [Google Scholar]
  43. 43.
    Galindo LJ, Torruella G, Moreira D, Eglit Y, Simpson AGB, et al. 2019.. Combined cultivation and single-cell approaches to the phylogenomics of nucleariid amoebae, close relatives of fungi. . Philos. Trans. R. Soc. B 374::20190094
    [Crossref] [Google Scholar]
  44. 44.
    Galindo LJ, Torruella G, Moreira D, Timpano H, Paskerova G, et al. 2018.. Evolutionary genomics of Metchnikovella incurvata (Metchnikovellidae): an early branching microsporidium. . Genome Biol. Evol. 10::273648
    [Crossref] [Google Scholar]
  45. 45.
    Garvetto A, Murúa P, Kirchmair M, Salvenmoser W, Hittorf M, et al. 2023.. Phagocytosis underpins the biotrophic lifestyle of intracellular parasites in the class Phytomyxea (Rhizaria). . New Phytol. 238::213043
    [Crossref] [Google Scholar]
  46. 46.
    Goodwin JD, Lee TF, Kugrens P, Simpson AGB. 2018.. Allobodo chlorophagus n. gen. n. sp., a kinetoplastid that infiltrates and feeds on the invasive alga Codium fragile. . Protist 169::91125
    [Crossref] [Google Scholar]
  47. 47.
    Guérin A, Roy NH, Kugler EM, Berry L, Burkhardt JK, et al. 2021.. Cryptosporidium rhoptry effector protein ROP1 injected during invasion targets the host cytoskeletal modulator LMO7. . Cell Host Microbe 29::140720.e5
    [Crossref] [Google Scholar]
  48. 48.
    Haag KL, James TY, Pombert J-F, Larsson R, Schaer TMM, et al. 2014.. Evolution of a morphological novelty occurred before genome compaction in a lineage of extreme parasites. . PNAS 111::1548085
    [Crossref] [Google Scholar]
  49. 49.
    Haag KL, Pombert JF, Sun YK, de Albuquerque NRM, Batliner B, et al. 2020.. Microsporidia with vertical transmission were likely shaped by nonadaptive processes. . Genome Biol. Evol. 12::3599614
    [Crossref] [Google Scholar]
  50. 50.
    Han B, Takvorian PM, Weiss LM. 2020.. Invasion of host cells by Microsporidia. . Front. Microbiol. 11::172
    [Crossref] [Google Scholar]
  51. 51.
    Harmer J, Yurchenko V, Nenarokova A, Lukeš J, Ginger ML. 2018.. Farming, slaving and enslavement: histories of endosymbioses during kinetoplastid evolution. . Parasitology 145::131123
    [Crossref] [Google Scholar]
  52. 52.
    Heinz E, Hacker C, Dean P, Mifsud J, Goldberg AV, et al. 2014.. Plasma membrane-located purine nucleotide transport proteins are key components for host exploitation by microsporidian intracellular parasites. . PLOS Pathog. 10::e1004547
    [Crossref] [Google Scholar]
  53. 53.
    Horta MF, Andrade LO, Martins-Duarte ÉS, Castro-Gomes T. 2020.. Cell invasion by intracellular parasites – the many roads to infection. . J. Cell Sci. 133::jcs232488
    [Crossref] [Google Scholar]
  54. 54.
    Jackson AP, Otto TD, Aslett M, Armstrong SD, Bringaud F, et al. 2016.. Kinetoplastid phylogenomics reveals the evolutionary innovations associated with the origins of parasitism. . Curr. Biol. 26::16172
    [Crossref] [Google Scholar]
  55. 55.
    James TY, Pelin A, Bonen L, Ahrendt S, Sain D, et al. 2013.. Shared signatures of parasitism and phylogenomics unite Cryptomycota and Microsporidia. . Curr. Biol. 23::154853
    [Crossref] [Google Scholar]
  56. 56.
    Janouškovec J, Paskerova GG, Miroliubova TS, Mikhailov KV, Birley T, et al. 2019.. Apicomplexan-like parasites are polyphyletic and widely but selectively dependent on cryptic plastid organelles. . eLife 8::e49662
    [Crossref] [Google Scholar]
  57. 57.
    Karpov SA, Mamkaeva MA, Aleoshin VV, Nassonova E, Lilje O, Gleason FH. 2014.. Morphology, phylogeny, and ecology of the aphelids (Aphelidea, Opisthokonta) and proposal for the new superphylum Opisthosporidia. . Front. Microbiol. 5::112
    [Crossref] [Google Scholar]
  58. 58.
    Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, et al. 2012.. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. . Bioinformatics 28::164749
    [Crossref] [Google Scholar]
  59. 59.
    Keeling PJ, Fast NM, Corradi N. 2014.. Microsporidian genome structure and function. . In Microsporidia: Pathogens of Opportunity, ed. LM Weiss, JJ Becnel , pp. 22129. Oxford, UK:: Wiley-Blackwell
    [Google Scholar]
  60. 60.
    Keeling PJ, McCutcheon JP. 2017.. Endosymbiosis: The feeling is not mutual. . J. Theor. Biol. 434::7579
    [Crossref] [Google Scholar]
  61. 61.
    Kishore SP, Stiller JW, Deitsch KW. 2013.. Horizontal gene transfer of epigenetic machinery and evolution of parasitism in the malaria parasite Plasmodium falciparum and other apicomplexans. . BMC Evol. Biol. 13::37
    [Crossref] [Google Scholar]
  62. 62.
    Kostygov AY, Karnkowska A, Votýpka J, Tashyreva D, Maciszewski K, et al. 2021.. Euglenozoa: taxonomy, diversity and ecology, symbioses and viruses. . Open Biol. 11::200407
    [Crossref] [Google Scholar]
  63. 63.
    Kwong WK, del Campo J, Mathur V, Vermeij MJA, Keeling PJ. 2019.. A widespread coral-infecting apicomplexan with chlorophyll biosynthesis genes. . Nature 568::1037
    [Crossref] [Google Scholar]
  64. 64.
    Larsson JIR. 2014.. The primitive Microsporidia. . In Microsporidia: Pathogens of Opportunity, ed. LM Weiss, JJ Becnel , pp. 60534. Oxford, UK:: Wiley-Blackwell
    [Google Scholar]
  65. 65.
    Lee YF, Cheng CC, Chen JS, Lin NN, Hung YW, et al. 2013.. Evidence of intracellular stages in Trypanosoma (Megatrypanum) theileri in non-phagocytic mammalian cells. . Vet. Parasitol. 191::22839
    [Crossref] [Google Scholar]
  66. 66.
    Lukeš J, Butenko A, Hashimi H, Maslov DA, Votýpka J, Yurchenko V. 2018.. Trypanosomatids are much more than just trypanosomes: clues from the expanded family tree. . Trends Parasitol. 34::46680
    [Crossref] [Google Scholar]
  67. 67.
    Lukeš J, Husník F. 2018.. Microsporidia: A single horizontal gene transfer drives a great leap forward. . Curr. Biol. 28::R71215
    [Crossref] [Google Scholar]
  68. 68.
    Lukeš J, Kachale A, Votýpka J, Butenko A, Field MC. 2022.. African trypanosome strategies for conquering new hosts and territories: the end of monophyly?. Trends Parasitol. 38::72436
    [Crossref] [Google Scholar]
  69. 69.
    Lukeš J, Skalický T, Týč J, Votýpka J, Yurchenko V. 2014.. Evolution of parasitism in kinetoplastid flagellates. . Mol. Biochem. Parasitol. 195::11522
    [Crossref] [Google Scholar]
  70. 70.
    Lukeš J, Speijer D, Zíková A, Alfonzo JD, Hashimi H, Field MC. 2023.. Trypanosomes as a magnifying glass for cell and molecular biology. . Trends Parasitol. 39::90212
    [Crossref] [Google Scholar]
  71. 71.
    Lukeš J, Wheeler R, Jirsová D, David V, Archibald JM. 2018.. Massive mitochondrial DNA content in diplonemid and kinetoplastid protists. . IUBMB Life 70::126774
    [Crossref] [Google Scholar]
  72. 72.
    Lutzoni F, Nowak MD, Alfaro ME, Reeb V, Miadlikowska J, et al. 2018.. Contemporaneous radiations of fungi and plants linked to symbiosis. . Nat. Commun. 9::5451
    [Crossref] [Google Scholar]
  73. 73.
    Mageswaran SK, Guérin A, Theveny LM, Chen WD, Martinez M, et al. 2021.. In situ ultrastructures of two evolutionarily distant apicomplexan rhoptry secretion systems. . Nat. Commun. 12::4983
    [Crossref] [Google Scholar]
  74. 74.
    Major P, Sendra KM, Dean P, Williams TA, Watson AK, et al. 2019.. A new family of cell surface located purine transporters in Microsporidia and related fungal endoparasites. . eLife 8::e47037
    [Crossref] [Google Scholar]
  75. 75.
    Manickavinayaham S, Dennehey BK, Johnson DG. 2021.. Direct regulation of DNA repair by E2F and RB in mammals and plants: core function or convergent evolution?. Cancers 13::934
    [Crossref] [Google Scholar]
  76. 76.
    Martin-Escolano J, Marín C, Rosales MJ, Tsaousis AD, Medina-Carmona E, Martin-Escolano R. 2022.. An updated view of the Trypanosoma cruzi life cycle: intervention points for an effective treatment. . ACS Infect. Dis. 8::110715
    [Crossref] [Google Scholar]
  77. 77.
    Maslov DA, Opperdoes FR, Kostygov AY, Hashimi H, Lukeš J, Yurchenko V. 2019.. Recent advances in trypanosomatid research: genome organization, expression, metabolism, taxonomy and evolution. . Parasitology 146::127
    [Crossref] [Google Scholar]
  78. 78.
    Mathur V, Kolísko M, Hehenberger E, Irwin NAT, Leander BS, et al. 2019.. Multiple independent origins of apicomplexan-like parasites. . Curr. Biol. 29::293641.e5
    [Crossref] [Google Scholar]
  79. 79.
    Mathur V, Salomaki ED, Wakeman KC, Na I, Kwong WK, et al. 2023.. Reconstruction of plastid proteomes of apicomplexans and close relatives reveals the major evolutionary outcomes of cryptic plastids. . Mol. Biol. Evol. 40::msad002
    [Crossref] [Google Scholar]
  80. 80.
    McBride JA, Gauthier GM, Klein BS. 2019.. Turning on virulence: mechanisms that underpin the morphologic transition and pathogenicity of Blastomyces. . Virulence 10::8019
    [Crossref] [Google Scholar]
  81. 81.
    Mendes TA, Lobo FP, Rodrigues TS, Rodrigues-Luiz GF, daRocha WD, et al. 2013.. Repeat-enriched proteins are related to host cell invasion and immune evasion in parasitic protozoa. . Mol. Biol. Evol. 30::95163
    [Crossref] [Google Scholar]
  82. 82.
    Mikhailov KV, Karpov SA, Letcher PM, Lee PA, Logacheva MD, et al. 2022.. Genomic analysis reveals cryptic diversity in aphelids and sheds light on the emergence of Fungi. . Curr. Biol. 32::460719.e7
    [Crossref] [Google Scholar]
  83. 83.
    Mikhailov KV, Simdyanov TG, Aleoshin VV. 2017.. Genomic survey of a hyperparasitic microsporidian Amphiamblys sp. (Metchnikovellidae). . Genome Biol. Evol. 9::45467
    [Google Scholar]
  84. 84.
    Mittal J, Ponce MG, Gendlina I, Nosanchuk JD. 2019.. Histoplasma capsulatum: mechanisms for pathogenesis. . In Fungal Physiology and Immunopathogenesis, Vol. 422, ed. ML Rodrigues , pp. 15791. Berlin:: Springer
    [Google Scholar]
  85. 85.
    Mohamed AR, Cumbo VR, Harii S, Shinzato C, Chan CX, et al. 2018.. Deciphering the nature of the coral–Chromera association. . ISME J. 12::77690
    [Crossref] [Google Scholar]
  86. 86.
    Moore RB, Oborník M, Janouškovec J, Chrudimský T, Vancová M, et al. 2008.. A photosynthetic alveolate closely related to apicomplexan parasites. . Nature 452::95963
    [Crossref] [Google Scholar]
  87. 87.
    Moreira D, López-García P, Vickerman K. 2004.. An updated view of kinetoplastid phylogeny using environmental sequences and a closer outgroup: proposal for a new classification of the class Kinetoplastea. . Int. J. Syst. Evol. Microbiol. 54::186175
    [Crossref] [Google Scholar]
  88. 88.
    Mukherjee I, Hodoki Y, Okazaki Y, Fujinaga S, Ohbayashi K, Nakano SI. 2019.. Widespread dominance of kinetoplastids and unexpected presence of diplonemids in deep freshwater lakes. . Front. Microbiol. 10::2375
    [Crossref] [Google Scholar]
  89. 89.
    Muñoz JF, Gauthier GM, Desjardins CA, Gallo JE, Holder J, et al. 2015.. The dynamic genome and transcriptome of the human fungal pathogen Blastomyces and close relative Emmonsia. . PLOS Genet. 11::e1005493
    [Crossref] [Google Scholar]
  90. 90.
    Muñoz-Gómez SA, Durnin K, Eme L, Paight C, Lane CE, et al. 2019.. Nephromyces represents a diverse and novel lineage of the Apicomplexa that has retained apicoplasts. . Genome Biol. Evol. 11::272740
    [Google Scholar]
  91. 91.
    Naranjo-Ortiz MA, Gabaldón T. 2019.. Fungal evolution: major ecological adaptations and evolutionary transitions. . Biol. Rev. 94::144376
    [Crossref] [Google Scholar]
  92. 92.
    Nowlin N, Smith I. 1917.. The intracellular development of a gregarine Frenzelina ampelisca n. sp. . J. Parasitol. 4::8388
    [Crossref] [Google Scholar]
  93. 93.
    Oborník M. 2019.. Endosymbiotic evolution of algae, secondary heterotrophy and parasitism. . Biomolecules 9::266
    [Crossref] [Google Scholar]
  94. 94.
    Oborník M. 2020.. Photoparasitism as an intermediate state in the evolution of apicomplexan parasites. . Trends Parasitol. 36::72734
    [Crossref] [Google Scholar]
  95. 95.
    Oborník M, Kručinská J, Esson H. 2016.. Life cycles of chromerids resemble those of colpodellids and apicomplexan parasites. . Perspect. Phycol. 3::2127
    [Google Scholar]
  96. 96.
    Oborník M, Lukeš J. 2015.. The organellar genomes of Chromera and Vitrella, the phototrophic relatives of apicomplexan parasites. . Annu. Rev. Microbiol. 69::12944
    [Crossref] [Google Scholar]
  97. 97.
    Oborník M, Vancová M, Lai D-H, Janouškovec J, Keeling PJ, Lukeš J. 2011.. Morphology and ultrastructure of multiple life cycle stages of the photosynthetic relative of Apicomplexa, Chromera velia. . Protist 162::11530
    [Crossref] [Google Scholar]
  98. 98.
    Ocaña-Pallarès E, Williams TA, López-Escardó D, Arroyo AS, Pathmanathan JS, et al. 2022.. Divergent genomic trajectories predate the origin of animals and fungi. . Nature 609::74753
    [Crossref] [Google Scholar]
  99. 99.
    Okamoto N, Inouye I. 2005.. The katablepharids are a distant sister group of the Cryptophyta: A proposal for Katablepharidophyta divisio nova/Kathablepharida phylum novum based on SSU rDNA and beta-tubulin phylogeny. . Protist 156::16379
    [Crossref] [Google Scholar]
  100. 100.
    Okamoto N, Keeling PJ. 2014.. The 3D structure of the apical complex and association with the flagellar apparatus revealed by serial TEM tomography in Psammosa pacifica, a distant relative of the Apicomplexa. . PLOS ONE 9::e84653
    [Crossref] [Google Scholar]
  101. 101.
    Okamoto N, McFadden GI. 2008.. The mother of all parasites. . Future Microbiol. 3::39195
    [Crossref] [Google Scholar]
  102. 102.
    Paskerova GG, Miroliubova TS, Diakin A, Kováčiková M, Valigurová A, et al. 2018.. Fine structure and molecular phylogenetic position of two marine gregarines, Selenidium pygospionis sp. n. and S. pherusae sp. n., with notes on the phylogeny of Archigregarinida (Apicomplexa). . Protist 169::82652
    [Crossref] [Google Scholar]
  103. 103.
    Pombert J-F, Selman M, Burki F, Bardell FT, Farinelli L, et al. 2012.. Gain and loss of multiple functionally related, horizontally transferred genes in the reduced genomes of two microsporidian parasites. . PNAS 109::1263843
    [Crossref] [Google Scholar]
  104. 104.
    Potter SC, Luciani A, Eddy SR, Park Y, Lopez R, Finn RD. 2018.. HMMER web server: 2018 update. . Nucleic Acids Res. 46::W2004
    [Crossref] [Google Scholar]
  105. 105.
    Poulin R, Randhawa HS. 2015.. Evolution of parasitism along convergent lines: from ecology to genomics. . Parasitology 142::S615
    [Crossref] [Google Scholar]
  106. 106.
    Quandt CA, Beaudet D, Corsaro D, Walochnik J, Michel R, et al. 2017.. The genome of an intranuclear parasite, Paramicrosporidium saccamoebae, reveals alternative adaptations to obligate intracellular parasitism. . eLife 6::e29594
    [Crossref] [Google Scholar]
  107. 107.
    Radek R, Kariton M, Dabert J, Alberti G. 2015.. Ultrastructural characterization of Acarispora falculifera n. gen., n. sp., a new microsporidium (Opisthokonta: Chytridiopsida) from the feather mite Falculifer rostratus (Astigmata: Pterolichoidea). . Acta Parasitol. 60::20010
    [Crossref] [Google Scholar]
  108. 108.
    Rueckert S, Betts EL, Tsaousis AD. 2019.. The symbiotic spectrum: Where do the gregarines fit?. Trends Parasitol. 35::68794
    [Crossref] [Google Scholar]
  109. 109.
    Sachs JL, Wilcox TP. 2006.. A shift to parasitism in the jellyfish symbiont Symbiodinium microadriaticum. . Proc. Biol. Sci. 273::42529
    [Google Scholar]
  110. 110.
    Saffo MB, McCoy AM, Rieken C, Slamovits CH. 2010.. Nephromyces, a beneficial apicomplexan symbiont in marine animals. . PNAS 107::1619095
    [Crossref] [Google Scholar]
  111. 111.
    Salomaki ED, Kolisko M. 2019.. There is treasure everywhere: reductive plastid evolution in Apicomplexa in light of their close relatives. . Biomolecules 9::378
    [Crossref] [Google Scholar]
  112. 112.
    Schoenle A, Hohlfeld M, Hermanns K, Mahé F, de Vargas C, et al. 2021.. High and specific diversity of protists in the deep-sea basins dominated by diplonemids, kinetoplastids, ciliates and foraminiferans. . Commun. Biol. 4::501
    [Crossref] [Google Scholar]
  113. 113.
    Seal S, Dharmarajan G, Khan I. 2021.. Evolution of pathogen tolerance and emerging infections: a missing experimental paradigm. . eLife 10::e68874
    [Crossref] [Google Scholar]
  114. 114.
    Sebghati TS, Engle JT, Goldman WE. 2000.. Intracellular parasitism by Histoplasma capsulatum: fungal virulence and calcium dependence. . Science 290::136872
    [Crossref] [Google Scholar]
  115. 115.
    Seto K, Matsuzawa T, Kuno H, Kagami M. 2020.. Morphology, ultrastructure, and molecular phylogeny of Aphelidium collabens sp. nov. (Aphelida), a parasitoid of a green alga Coccomyxa sp. . Protist 171::125728
    [Crossref] [Google Scholar]
  116. 116.
    Sheppard DC, Filler SG. 2015.. Host cell invasion by medically important fungi. . Cold Spring Harb. Perspect. Med. 5::a019687
    [Crossref] [Google Scholar]
  117. 117.
    Sibbald SJ, Cenci U, Colp M, Eglit Y, O'Kelly CJ, Archibald JM. 2017.. Diversity and evolution of Paramoeba spp. and their kinetoplastid endosymbionts. . J. Eukaryot. Microbiol. 64::598607
    [Crossref] [Google Scholar]
  118. 118.
    Sibley LD. 2011.. Invasion and intracellular survival by protozoan parasites. . Immunol. Rev. 240::7291
    [Crossref] [Google Scholar]
  119. 119.
    Sokol-Borrelli SL, Coombs RS, Boyle JP. 2020.. A comparison of stage conversion in the coccidian apicomplexans Toxoplasma gondii, Hammondia hammondi, and Neospora caninum. . Front. Cell. Infect. Microbiol. 10::608283
    [Crossref] [Google Scholar]
  120. 120.
    Sole R. 2022.. Revisiting Leigh Van Valen's “A New Evolutionary Law” (1973). . Biol. Theory 17::12025
    [Crossref] [Google Scholar]
  121. 121.
    Somerville V, Berthoud H, Schmidt RS, Bachmann HP, Meng YH, et al. 2022.. Functional strain redundancy and persistent phage infection in Swiss hard cheese starter cultures. . ISME J. 16::38899
    [Crossref] [Google Scholar]
  122. 122.
    Suss-Toby E, Zimmerberg J, Ward GE. 1996.. Toxoplasma invasion: The parasitophorous vacuole is formed from host cell plasma membrane and pinches off via a fission pore. . PNAS 93::841318
    [Crossref] [Google Scholar]
  123. 123.
    Tamim El Jarkass H, Reinke AW. 2020.. The ins and outs of host-microsporidia interactions during invasion, proliferation and exit. . Cell. Microbiol. 22::e13247
    [Crossref] [Google Scholar]
  124. 124.
    Tanifuji G, Cenci U, Moog D, Dean S, Nakayama T, et al. 2017.. Genome sequencing reveals metabolic and cellular interdependence in an amoeba-kinetoplastid symbiosis. . Sci. Rep. 7::11688
    [Crossref] [Google Scholar]
  125. 125.
    Tikhonenkov DV, Gawryluk RMR, Mylnikov AP, Keeling PJ. 2021.. First finding of free-living representatives of Prokinetoplastina and their nuclear and mitochondrial genomes. . Sci. Rep. 11::2946
    [Crossref] [Google Scholar]
  126. 126.
    Timofeev S, Tokarev Y, Dolgikh V. 2020.. Energy metabolism and its evolution in Microsporidia and allied taxa. . Parasitol. Res. 119::143341
    [Crossref] [Google Scholar]
  127. 127.
    Torruella G, Grau-Bové X, Moreira D, Karpov SA, Burns JA, et al. 2018.. Global transcriptome analysis of the aphelid Paraphelidium tribonemae supports the phagotrophic origin of fungi. . Commun. Biol. 1::231
    [Crossref] [Google Scholar]
  128. 128.
    Tsaousis AD, Kunji ERS, Goldberg AV, Lucocq JM, Hirt RP, Embley TM. 2008.. A novel route for ATP acquisition by the remnant mitochondria of Encephalitozoon cuniculi. . Nature 453::55356
    [Crossref] [Google Scholar]
  129. 129.
    van de Vossenberg BTLH, Warris S, Nguyen HDT, van Gent-Pelzer MPE, Joly DL, et al. 2019.. Comparative genomics of chytrid fungi reveal insights into the obligate biotrophic and pathogenic lifestyle of Synchytrium endobioticum. . Sci. Rep. 9::8672
    [Crossref] [Google Scholar]
  130. 130.
    Vávra J, Lukeš J. 2013.. Microsporidia and ‘the art of living together. .’ Adv. Parasitol. 82::253319
    [Crossref] [Google Scholar]
  131. 131.
    Votýpka J, Modrý D, Oborník M, Šlapeta J, Lukeš J. 2017.. Apicomplexa. . In Handbook of the Protists, ed. JM Archibald, AGB Simpson, CH Slamovits , pp. 567624. Cham, Switz:.: Springer
    [Google Scholar]
  132. 132.
    Wadi L, Reinke AW. 2020.. Evolution of microsporidia: an extremely successful group of eukaryotic intracellular parasites. . PLOS Pathog. 16::e1008276
    [Crossref] [Google Scholar]
  133. 133.
    Weinstein SB, Kuris AM. 2016.. Independent origins of parasitism in Animalia. . Biol. Lett. 12::20160324
    [Crossref] [Google Scholar]
  134. 134.
    Whelan TA, Lee NT, Lee RCH, Fast NM. 2019.. Microsporidian introns retained against a background of genome reduction: characterization of an unusual set of introns. . Genome Biol. Evol. 11::26369
    [Crossref] [Google Scholar]
  135. 135.
    Williams BAP, Hirt RP, Lucocq JM, Embley TM. 2002.. A mitochondrial remnant in the microsporidian Trachipleistophora hominis. . Nature 418::86569
    [Crossref] [Google Scholar]
  136. 136.
    Wolf YI, Koonin EV. 2013.. Genome reduction as the dominant mode of evolution. . Bioessays 35::82937
    [Crossref] [Google Scholar]
  137. 137.
    Woo YH, Ansari H, Otto TD, Klinger CM, Kolisko M, et al. 2015.. Chromerid genomes reveal the evolutionary path from photosynthetic algae to obligate intracellular parasites. . eLife 4::e06974
    [Crossref] [Google Scholar]
  138. 138.
    Wu BJ, Hao WL, Cox MP. 2022.. Reconstruction of gene innovation associated with major evolutionary transitions in the kingdom Fungi. . BMC Biol. 20::144
    [Crossref] [Google Scholar]
  139. 139.
    Yazaki E, Ishikawa SA, Kume K, Kumagai A, Kamaishi T, et al. 2017.. Global Kinetoplastea phylogeny inferred from a large-scale multigene alignment including parasitic species for better understanding transitions from a free-living to a parasitic lifestyle. . Genes Genet. Syst. 92::3542
    [Crossref] [Google Scholar]
  140. 140.
    Yuan CL, Keeling PJ, Krause PJ, Horak A, Bent S, et al. 2012.. Colpodella spp.–like parasite infection in woman, China. . Emerg. Infect. Dis. 18::12527
    [Crossref] [Google Scholar]
  141. 141.
    Žárský V, Karnkowska A, Boscaro V, Trznadel M, Whelan TA, et al. 2023.. Contrasting outcomes of genome reduction in mikrocytids and microsporidians. . BMC Biol. 21::137
    [Crossref] [Google Scholar]
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