1932

Abstract

Ciliates are a diverse group of unicellular eukaryotes that vary widely in size, shape, body plan, and ecological niche. Here, we review recent research advances achieved with ciliate models. Studies on patterning and regeneration have been revived in the giant ciliate , facilitated by modern omics methods. Cryo-electron microscopy and tomography have revolutionized the structural study of complex macromolecules such as telomerase, ribozymes, and axonemes. DNA elimination, gene scrambling, and mating type determination have been deciphered, revealing interesting adaptations of processes that have parallels in other kingdoms of life. Studies of common eukaryotic processes, such as intracellular trafficking, meiosis, and histone modification, reveal conservation as well as unique adaptations in these organisms that are evolutionarily distant from other models. Continual improvement of genetic and molecular tools makes ciliates accessible models for all levels of education and research. Such advances open new avenues of research and highlight the importance of ciliate research.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-cellbio-120420-020656
2022-10-06
2024-04-24
Loading full text...

Full text loading...

/deliver/fulltext/cellbio/38/1/annurev-cellbio-120420-020656.html?itemId=/content/journals/10.1146/annurev-cellbio-120420-020656&mimeType=html&fmt=ahah

Literature Cited

  1. Adoutte A, Ling KY, Forte M, Ramanathan R, Nelson D, Kung C 1981. Ionic channels of Paramecium: from genetics and electrophysiology to biochemistry. J. Physiol. 77:91145–59 https://pubmed.ncbi.nlm.nih.gov/6286966/
    [Google Scholar]
  2. Aeschlimann SH, Jönsson F, Postberg J, Stover NA, Petera RL et al. 2014. The draft assembly of the radically organized Stylonychia lemnae macronuclear genome. Genome Biol. Evol. 6:71707–23 https://doi.org/10.1093/gbe/evu139
    [Crossref] [Google Scholar]
  3. Ali EI, Loidl J, Howard-Till RA. 2018. A streamlined cohesin apparatus is sufficient for mitosis and meiosis in the protist Tetrahymena. Chromosoma 127:4421–35 https://doi.org/10.1007/s00412-018-0673-x
    [Crossref] [Google Scholar]
  4. Alimenti C, Buonanno F, Di Giuseppe G, Guella G, Luporini P et al. 2022. Bioactive molecules from ciliates: structure, activity, and applicative potential. J. Eukaryot. Microbiol. 00:e12887 https://doi.org/10.1111/jeu.12887
    [Crossref] [Google Scholar]
  5. Allen RD. 1969. The morphogenesis of basal bodies and accessory structures of the cortex of the ciliated protozoan Tetrahymena pyriformis. J. Cell Biol. 40:3716–33 https://doi.org/10.1083/jcb.40.3.716
    [Crossref] [Google Scholar]
  6. Allen SE, Nowacki M 2020. Roles of noncoding RNAs in ciliate genome architecture. J. Mol. Biol. 432:154186–98 https://doi.org/10.1016/j.jmb.2019.12.042
    [Crossref] [Google Scholar]
  7. Arnaiz O, Meyer E, Sperling L 2020. ParameciumDB 2019: integrating genomic data across the genus for functional and evolutionary biology. Nucleic Acids Res 48:D1D599–605 https://doi.org/10.1093/nar/gkz948
    [Crossref] [Google Scholar]
  8. Ashraf K, Nabeel-Shah S, Garg J, Saettone A, Derynck J et al. 2019. Proteomic analysis of histones H2A/H2B and variant Hv1 in Tetrahymena thermophila reveals an ancient network of chaperones. Mol. Biol. Evol. 36:51037–55 https://doi.org/10.1093/molbev/msz039
    [Crossref] [Google Scholar]
  9. Aubusson-Fleury A, Balavoine G, Lemullois M, Bouhouche K, Beisson J, Koll F. 2017. Centrin diversity and basal body patterning across evolution: new insights from Paramecium. Biol. Open 6:6765–76 https://doi.org/10.1242/bio.024273
    [Crossref] [Google Scholar]
  10. Aury J-M, Jaillon O, Duret L, Noel B, Jubin C et al. 2006. Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia. Nature 444:7116171–78 https://doi.org/10.1038/nature05230
    [Crossref] [Google Scholar]
  11. Bastiaanssen C, Joo C. 2021. Small RNA-directed DNA elimination: the molecular mechanism and its potential for genome editing. RNA Biol 18:111540–45 https://doi.org/10.1080/15476286.2021.1885208
    [Crossref] [Google Scholar]
  12. Bayless BA, Navarro FM, Winey M. 2019. Motile cilia: innovation and insight from ciliate model organisms. Front. Cell Dev. Biol. 7:265 https://doi.org/10.3389/fcell.2019.00265
    [Crossref] [Google Scholar]
  13. Beales PL, Bland E, Tobin JL, Bacchelli C, Tuysuz B et al. 2007. IFT80, which encodes a conserved intraflagellar transport protein, is mutated in Jeune asphyxiating thoracic dystrophy. Nat. Genet. 39:6727–29 https://doi.org/10.1038/ng2038
    [Crossref] [Google Scholar]
  14. Beh LY, Debelouchina GT, Clay DM, Thompson RE, Lindblad KA et al. 2019. Identification of a DNA N6-adenine methyltransferase complex and its impact on chromatin organization. Cell 177:71781–96.e25 https://doi.org/10.1016/j.cell.2019.04.028
    [Crossref] [Google Scholar]
  15. Bengueddach H, Lemullois M, Aubusson-Fleury A, Koll F 2017. Basal body positioning and anchoring in the multiciliated cell Paramecium tetraurelia: roles of OFD1 and VFL3. Cilia 6:6 https://doi.org/10.1186/s13630-017-0050-z
    [Crossref] [Google Scholar]
  16. Bondarenko VS, Gelfand MS. 2016. Evolution of the exon-intron structure in ciliate genomes. PLOS ONE 11:9e0161476 https://doi.org/10.1371/journal.pone.0161476
    [Crossref] [Google Scholar]
  17. Bouhouche K, Valentine MS, Le Borgne P, Lemullois M, Yano J et al. 2022. Paramecium, a model to study ciliary beating and ciliogenesis: insights from cutting-edge approaches. Front. Cell Dev. Biol. 10: https://doi.org/10.3389/fcell.2022.847908
    [Crossref] [Google Scholar]
  18. Bracht JR, Perlman DH, Landweber LF. 2012. Cytosine methylation and hydroxymethylation mark DNA for elimination in Oxytricha trifallax. Genome Biol 13:10R99 https://doi.org/10.1186/gb-2012-13-10-r99
    [Crossref] [Google Scholar]
  19. Bright LJ, Gout J-F, Lynch M. 2017. Early stages of functional diversification in the Rab GTPase gene family revealed by genomic and localization studies in Paramecium species. Mol. Biol. Cell 28:81101–10 https://doi.org/10.1091/MBC.E16-06-0361
    [Crossref] [Google Scholar]
  20. Bright LJ, Kambesis N, Nelson SB, Jeong B, Turkewitz AP. 2010. Comprehensive analysis reveals dynamic and evolutionary plasticity of Rab GTPases and membrane traffic in Tetrahymena thermophila. PLOS Genet 6:10e1001155 https://doi.org/10.1371/JOURNAL.PGEN.1001155
    [Crossref] [Google Scholar]
  21. Bright LJ, Lynch M. 2020. The Rab7 subfamily across Paramecium aurelia species; evidence of high conservation in sequence and function. Small GTPases 11:6421–29 https://doi.org/10.1080/21541248.2018.1502056
    [Crossref] [Google Scholar]
  22. Cervantes MD, Hamilton EP, Xiong J, Lawson MJ, Yuan D et al. 2013. Selecting one of several mating types through gene segment joining and deletion in Tetrahymena thermophila. PLOS Biol 11:3e1001518 https://doi.org/10.1371/journal.pbio.1001518
    [Crossref] [Google Scholar]
  23. Chalker DL 2012. Transformation and strain engineering of Tetrahymena. Tetrahymena thermophila ed. K Collins pp. 32745 Methods Cell Biol. 109. Waltham, MA: Academic
    [Google Scholar]
  24. Chalker DL, Meyer E, Mochizuki K 2013. Epigenetics of ciliates. Cold Spring Harb. Perspect. Biol. 5:12a017764 https://doi.org/10.1101/cshperspect.a017764
    [Crossref] [Google Scholar]
  25. Chen W, Zuo C, Wang C, Zhang T, Lyu L et al. 2021. The hidden genomic diversity of ciliated protists revealed by single-cell genome sequencing. BMC Biol 19:1264 https://doi.org/10.1186/s12915-021-01202-1
    [Crossref] [Google Scholar]
  26. Chen X, Bracht JR, Goldman AD, Dolzhenko E, Clay DM et al. 2014. The architecture of a scrambled genome reveals massive levels of genomic rearrangement during development. Cell 158:51187–98 https://doi.org/10.1016/j.cell.2014.07.034
    [Crossref] [Google Scholar]
  27. Chen X, Jiang Y, Gao F, Zheng W, Krock TJ et al. 2019. Genome analyses of the new model protist Euplotes vannus focusing on genome rearrangement and resistance to environmental stressors. Mol. Ecol. Resourc. 19:51292–308 https://doi.org/10.1111/1755-0998.13023
    [Crossref] [Google Scholar]
  28. Chen X, Jung S, Beh LY, Eddy SR, Landweber LF. 2015. Combinatorial DNA rearrangement facilitates the origin of new genes in ciliates. Genome Biol. Evol. 7:102859–70 https://doi.org/10.1093/gbe/evv172
    [Crossref] [Google Scholar]
  29. Clamp JC, Lynn DH. 2017. Investigating the biodiversity of ciliates in the ‘Age of Integration.’. Eur. J. Protistol. 61:Part B314–22 https://doi.org/10.1016/j.ejop.2017.01.004
    [Crossref] [Google Scholar]
  30. Cole E, Gaertig J 2022. Anterior-posterior pattern formation in ciliates. J. Eukaryot. Microbiol. 00:e12890 https://doi.org/10.1111/jeu.12890
    [Crossref] [Google Scholar]
  31. Couvillion MT, Collins K 2012. Biochemical approaches including the design and use of strains expressing epitope-tagged proteins. Tetrahymena thermophila ed. K Collins pp. 34755 Methods Cell Biol. 109. Waltham, MA: Academic
    [Google Scholar]
  32. Coyne RS, Hannick L, Shanmugam D, Hostetler JB, Brami D et al. 2011. Comparative genomics of the pathogenic ciliate Ichthyophthirius multifiliis, its free-living relatives and a host species provide insights into adoption of a parasitic lifestyle and prospects for disease control. Genome Biol 12:10R100 https://doi.org/10.1186/gb-2011-12-10-r100
    [Crossref] [Google Scholar]
  33. Coyne RS, Thiagarajan M, Jones KM, Wortman JR, Tallon LJ et al. 2008. Refined annotation and assembly of the Tetrahymena thermophila genome sequence through EST analysis, comparative genomic hybridization, and targeted gap closure. BMC Genom. 9:562 https://doi.org/10.1186/1471-2164-9-562
    [Crossref] [Google Scholar]
  34. Dekker J, Marti-Renom MA, Mirny LA. 2013. Exploring the three-dimensional organization of genomes: interpreting chromatin interaction data. Nat. Rev. Genet. 14:6390–403 https://doi.org/10.1038/nrg3454
    [Crossref] [Google Scholar]
  35. Dippell RV. 1968. The development of basal bodies in Paramecium. PNAS 61:2461–68 https://doi.org/10.1073/pnas.61.2.461
    [Crossref] [Google Scholar]
  36. Docampo R, Moreno SNJ, Plattner H. 2014. Intracellular calcium channels in protozoa. Eur. J. Pharmacol. 739:4–18 https://doi.org/10.1016/J.EJPHAR.2013.11.015
    [Crossref] [Google Scholar]
  37. Eckert R, Brehm P. 1979. Ionic mechanisms of excitation in Paramecium. Annu. Rev. Biophys. Bioeng. 8:353–83 https://doi.org/10.1146/annurev.bb.08.060179.002033
    [Crossref] [Google Scholar]
  38. Eisen JA, Coyne RS, Wu M, Wu D, Thiagarajan M et al. 2006. Macronuclear genome sequence of the ciliate Tetrahymena thermophila, a model eukaryote. PLOS Biol 4:9e286 https://doi.org/10.1371/journal.pbio.0040286
    [Crossref] [Google Scholar]
  39. Elde NC, Morgan G, Winey M, Sperling L, Turkewitz AP. 2005. Elucidation of clathrin-mediated endocytosis in Tetrahymena reveals an evolutionarily convergent recruitment of dynamin. PLOS Genet 1:5e52 https://doi.org/10.1371/JOURNAL.PGEN.0010052
    [Crossref] [Google Scholar]
  40. Fabritius AS, Bayless BA, Li S, Stoddard D, Heydeck W et al. 2021. Proteomic analysis of microtubule inner proteins (MIPs) in Rib72 null Tetrahymena cells reveals functional MIPs. Mol. Biol. Cell 32:21br8 https://doi.org/10.1091/mbc.E20-12-0786
    [Crossref] [Google Scholar]
  41. Feng L, Wang G, Hamilton EP, Xiong J, Yan G et al. 2017. A germline-limited PiggyBac transposase gene is required for precise excision in Tetrahymena genome rearrangement. Nucleic Acids Res 45:169481–502 https://doi.org/10.1093/nar/gkx652
    [Crossref] [Google Scholar]
  42. Fokin SI. 2004. A brief history of ciliate studies (late XVII - the first third of the XX century). Protistology 3:4283–96
    [Google Scholar]
  43. Fu G, Wang Q, Phan N, Urbanska P, Joachimiak E et al. 2018. The I1 dynein-associated tether and tether head complex is a conserved regulator of ciliary motility. Mol. Biol. Cell 29:91048–59 https://doi.org/10.1091/mbc.E18-02-0142
    [Crossref] [Google Scholar]
  44. Galati DF, Bonney S, Kronenberg Z, Clarissa C, Yandell M et al. 2014. DisAp-dependent striated fiber elongation is required to organize ciliary arrays. J. Cell Biol. 207:6705–15 https://doi.org/10.1083/jcb.201409123
    [Crossref] [Google Scholar]
  45. Galione A, Evans AM, Ma J, Parrington J, Arredouani A et al. 2009. The acid test: the discovery of two-pore channels (TPCs) as NAADP-gated endolysosomal Ca2+ release channels. Eur. J. Physiol. 458:5869–76 https://doi.org/10.1007/S00424-009-0682-Y
    [Crossref] [Google Scholar]
  46. Galvani A, Sperling L. 2002. RNA interference by feeding in Paramecium. Trends Genet. 18:111–12 https://doi.org/10.1016/s0168-9525(01)02548-3
    [Crossref] [Google Scholar]
  47. Gout J-F, Lynch M. 2015. Maintenance and loss of duplicated genes by dosage subfunctionalization. Mol. Biol. Evol. 32:82141–48 https://doi.org/10.1093/molbev/msv095
    [Crossref] [Google Scholar]
  48. Greenwood SJ, Sogin ML, Lynn DH. 1991. Phylogenetic relationships within the class Oligohymenophorea, phylum Ciliophora, inferred from the complete small subunit rRNA gene sequences of Colpidium campylum, Glaucoma chattoni, and Opisthonecta henneguyi. J. Mol. Evol. 33:2163–74 https://doi.org/10.1007/BF02193631
    [Crossref] [Google Scholar]
  49. Guérin F, Arnaiz O, Boggetto N, Wilkes CD, Meyer E et al. 2017. Flow cytometry sorting of nuclei enables the first global characterization of Paramecium germline DNA and transposable elements. BMC Genom 18:1327 https://doi.org/10.1186/s12864-017-3713-7
    [Crossref] [Google Scholar]
  50. Guerrier S, Plattner H, Richardson E, Dacks JB, Turkewitz AP. 2017. An evolutionary balance: conservation versus innovation in ciliate membrane trafficking. Traffic 18:118–28 https://doi.org/10.1111/tra.12450
    [Crossref] [Google Scholar]
  51. Gui M, Farley H, Anujan P, Anderson JR, Maxwell DW et al. 2021. De novo identification of mammalian ciliary motility proteins using cryo-EM. Cell 184:235791–806.e19 https://doi.org/10.1016/j.cell.2021.10.007
    [Crossref] [Google Scholar]
  52. Hamilton EP, Kapusta A, Huvos PE, Bidwell SL, Zafar N et al. 2016. Structure of the germline genome of Tetrahymena thermophila and relationship to the massively rearranged somatic genome. eLife 5:e19090 https://doi.org/10.7554/eLife.19090
    [Crossref] [Google Scholar]
  53. Hayashi A, Mochizuki K. 2015. Targeted gene disruption by ectopic induction of DNA elimination in Tetrahymena. Genetics 201:155–64 https://doi.org/10.1534/genetics.115.178525
    [Crossref] [Google Scholar]
  54. He Y, Wang Y, Liu B, Helmling C, Sušac L et al. 2021. Structures of telomerase at several steps of telomere repeat synthesis. Nature 593:7859454–59 https://doi.org/10.1038/s41586-021-03529-9
    [Crossref] [Google Scholar]
  55. Heaphy SM, Mariotti M, Gladyshev VN, Atkins JF, Baranov PV. 2016. Novel ciliate genetic code variants including the reassignment of all three stop codons to sense codons in Condylostoma magnum. Mol. Biol. Evol. 33:112885–89 https://doi.org/10.1093/molbev/msw166
    [Crossref] [Google Scholar]
  56. Howard-Till RA, Loidl J 2018. Condensins promote chromosome individualization and segregation during mitosis, meiosis, and amitosis in Tetrahymena thermophila. Mol. Biol. Cell 29:4466–78 https://doi.org/10.1091/mbc.E17-07-0451
    [Crossref] [Google Scholar]
  57. Howard-Till RA, Lukaszewicz A, Novatchkova M, Loidl J. 2013. A single cohesin complex performs mitotic and meiotic functions in the protist Tetrahymena. PLOS Genet 9:3e1003418 https://doi.org/10.1371/journal.pgen.1003418
    [Crossref] [Google Scholar]
  58. Howard-Till RA, Tian M, Loidl J. 2019. A specialized condensin complex participates in somatic nuclear maturation in Tetrahymena thermophila. Mol. Biol. Cell 30:111326–38 https://doi.org/10.1091/mbc.E18-08-0487
    [Crossref] [Google Scholar]
  59. Howard-Till RA, Yao M-C. 2006. Induction of gene silencing by hairpin RNA expression in Tetrahymena thermophila reveals a second small RNA pathway. Mol. Cell. Biol. 26:238731–42 https://doi.org/10.1128/MCB.01430-06
    [Crossref] [Google Scholar]
  60. Huang B, Pitelka DR. 1973. The contractile process in the ciliate, Stentor coeruleus. I. The role of microtubules and filaments. J. Cell Biol. 57:3704–28 https://doi.org/10.1083/jcb.57.3.704
    [Crossref] [Google Scholar]
  61. Hufnagel LA. 2022. The cilioprotist cytoskeleton, a model for understanding how cell architecture and pattern are specified: recent discoveries from ciliates and comparable model systems. Methods Mol. Biol. 2364.251–95 https://doi.org/10.1007/978-1-0716-1661-1_13
    [Crossref] [Google Scholar]
  62. Huotari J, Helenius A. 2011. Endosome maturation. EMBO J 30:173481–500 https://doi.org/10.1038/EMBOJ.2011.286
    [Crossref] [Google Scholar]
  63. Ichikawa M, Bui KH. 2018. Microtubule inner proteins: a meshwork of luminal proteins stabilizing the doublet microtubule. BioEssays 40:3e1700209 https://doi.org/10.1002/bies.201700209
    [Crossref] [Google Scholar]
  64. Ichikawa M, Khalifa AAZ, Kubo S, Dai D, Basu K et al. 2019. Tubulin lattice in cilia is in a stressed form regulated by microtubule inner proteins. PNAS 116:4019930–38 https://doi.org/10.1073/pnas.1911119116
    [Crossref] [Google Scholar]
  65. Ichikawa M, Liu D, Kastritis PL, Basu K, Hsu TC et al. 2017. Subnanometre-resolution structure of the doublet microtubule reveals new classes of microtubule-associated proteins. Nat. Commun. 8:15035 https://doi.org/10.1038/ncomms15035
    [Crossref] [Google Scholar]
  66. Ishikawa T. 2015. Cryo-electron tomography of motile cilia and flagella. Cilia 4:3 https://doi.org/10.1186/s13630-014-0012-7
    [Crossref] [Google Scholar]
  67. Jacobs ME, DeSouza LV, Samaranayake H, Pearlman RE, Siu KWM, Klobutcher LA. 2006. The Tetrahymena thermophila phagosome proteome. Eukaryot. Cell 5:121990–2000 https://doi.org/10.1128/EC.00195-06
    [Crossref] [Google Scholar]
  68. Jiang J, Chan H, Cash DD, Miracco EJ, Loo RRO et al. 2015. Structure of Tetrahymena telomerase reveals previously unknown subunits, functions, and interactions. Science 350:6260aab4070 https://doi.org/10.1126/science.aab4070
    [Crossref] [Google Scholar]
  69. Jiang Y-Y, Maier W, Baumeister R, Minevich G, Joachimiak E et al. 2017. The Hippo pathway maintains the equatorial division plane in the ciliate Tetrahymena. Genetics 206:2873–88 https://doi.org/10.1534/genetics.117.200766
    [Crossref] [Google Scholar]
  70. Joachimiak E, Osinka A, Farahat H, Świderska B, Sitkiewicz E et al. 2021. Composition and function of the C1b/C1f region in the ciliary central apparatus. Sci. Rep. 11:11760 https://doi.org/10.1038/s41598-021-90996-9
    [Crossref] [Google Scholar]
  71. Johri P, Krenek S, Marinov GK, Doak TG, Berendonk TU, Lynch M. 2017. Population genomics of Paramecium species. Mol. Biol. Evol. 34:51194–216 https://doi.org/10.1093/molbev/msx074
    [Crossref] [Google Scholar]
  72. Johri P, Marinov GK, Doak TG, Lynch M. 2019. Population genetics of Paramecium mitochondrial genomes: recombination, mutation spectrum, and efficacy of selection. Genome Biol. Evol. 11:51398–416 https://doi.org/10.1093/gbe/evz081
    [Crossref] [Google Scholar]
  73. Jumper J, Evans R, Pritzel A, Green T, Figurnov M et al. 2021. Highly accurate protein structure prediction with AlphaFold. Nature 596:7873583–89 https://doi.org/10.1038/s41586-021-03819-2
    [Crossref] [Google Scholar]
  74. Junker AD, Soh AWJ, O'Toole ET, Meehl JB, Guha M et al. 2019. Microtubule glycylation promotes attachment of basal bodies to the cell cortex. J. Cell Sci. 132:15jcs233726 https://doi.org/10.1242/jcs.233726
    [Crossref] [Google Scholar]
  75. Juranek S, Wieden H-J, Lipps HJ. 2003. De novo cytosine methylation in the differentiating macronucleus of the stichotrichous ciliate Stylonychia lemnae. Nucleic Acids Res 31:51387–91 https://doi.org/10.1093/nar/gkg233
    [Crossref] [Google Scholar]
  76. Kar UP, Dey H, Rahaman A. 2021. Cardiolipin targets a dynamin-related protein to the nuclear membrane. eLife 10:e64416 https://doi.org/10.7554/eLife.64416
    [Crossref] [Google Scholar]
  77. Khalifa AAZ, Ichikawa M, Dai D, Kubo S, Black CS et al. 2020. The inner junction complex of the cilia is an interaction hub that involves tubulin post-translational modifications. eLife 9:e52760 https://doi.org/10.7554/eLife.52760
    [Crossref] [Google Scholar]
  78. Kilburn CL, Pearson CG, Romijn EP, Meehl JB, Giddings TH et al. 2007. New Tetrahymena basal body protein components identify basal body domain structure. J. Cell Biol. 178:6905–12 https://doi.org/10.1083/jcb.200703109
    [Crossref] [Google Scholar]
  79. Klena N, Le Guennec M, Tassin A-M, van den Hoek H, Erdmann PS et al. 2020. Architecture of the centriole cartwheel-containing region revealed by cryo-electron tomography. EMBO J 39:22e106246 https://doi.org/10.15252/embj.2020106246
    [Crossref] [Google Scholar]
  80. Kontur C, Kumar S, Lan X, Pritchard JK, Turkewitz AP. 2016. Whole genome sequencing identifies a novel factor required for secretory granule maturation in Tetrahymena thermophila. G3 6:82505–16 https://doi.org/10.1534/g3.116.028878
    [Crossref] [Google Scholar]
  81. Ladenburger E-M, Plattner H. 2011. Calcium-release channels in Paramecium. Genomic expansion, differential positioning and partial transcriptional elimination. PLOS ONE 6:11e27111 https://doi.org/10.1371/JOURNAL.PONE.0027111
    [Crossref] [Google Scholar]
  82. Ladenburger E-M, Sehring IM, Korn I, Plattner H. 2009. Novel types of Ca2+ release channels participate in the secretory cycle of Paramecium cells. Mol. Cell. Biol. 29:133605–22 https://doi.org/10.1128/MCB.01592-08
    [Crossref] [Google Scholar]
  83. Lee SR, Collins K. 2006. Two classes of endogenous small RNAs in Tetrahymena thermophila. Genes Dev 20:128–33 https://doi.org/10.1101/gad.1377006
    [Crossref] [Google Scholar]
  84. Lee SR, Collins K. 2007. Physical and functional coupling of RNA-dependent RNA polymerase and dicer in the biogenesis of endogenous siRNAs. Nat. Struct. Mol. Biol. 14:7604–10 https://doi.org/10.1038/nsmb1262
    [Crossref] [Google Scholar]
  85. Lee SR, Pollard DA, Galati DF, Kelly ML, Miller B et al. 2021. Disruption of a ∼23–24 nucleotide small RNA pathway elevates DNA damage responses in Tetrahymena thermophila. Mol. Biol. Cell 32:151335–46 https://doi.org/10.1091/mbc.E20-10-0631
    [Crossref] [Google Scholar]
  86. Lee SR, Talsky KB, Collins K. 2009. A single RNA-dependent RNA polymerase assembles with mutually exclusive nucleotidyl transferase subunits to direct different pathways of small RNA biogenesis. RNA 15:71363–74 https://doi.org/10.1261/rna.1630309
    [Crossref] [Google Scholar]
  87. Li C, Chen X, Zheng W, Doak TG, Fan G et al. 2021. Chromosome organization and gene expansion in the highly fragmented genome of the ciliate Strombidium stylifer. J. Genet. Genom. 48:10908–16 https://doi.org/10.1016/j.jgg.2021.05.014
    [Crossref] [Google Scholar]
  88. Li S, Fernandez J-J, Fabritius AS, Agard DA, Winey M 2022. Electron cryo-tomography structure of axonemal doublet microtubule from Tetrahymena thermophila. Life Sci. Alliance 5:3e202101225 https://doi.org/10.26508/lsa.202101225
    [Crossref] [Google Scholar]
  89. Lin A, Makushok T, Diaz U, Marshall WF. 2018. Methods for the study of regeneration in Stentor. J. Visualized Exp. 136:e57759 https://doi.org/10.3791/57759
    [Crossref] [Google Scholar]
  90. Lin A, Piehowski PD, Tsai C-F, Makushok T, L Yi et al. 2022. Proteomic dissection of a giant cell. bioRxiv 475287 https://doi.org/10.1101/2022.01.06.475287
    [Crossref]
  91. Lin I-T, Yao M-C. 2020. Selfing mutants link Ku proteins to mating type determination in Tetrahymena. PLOS Biol 18:8e3000756 https://doi.org/10.1371/journal.pbio.3000756
    [Crossref] [Google Scholar]
  92. Loidl J. 2021. Tetrahymena meiosis: simple yet ingenious. PLOS Genet 17:7e1009627 https://doi.org/10.1371/journal.pgen.1009627
    [Crossref] [Google Scholar]
  93. Loidl J, Scherthan H. 2004. Organization and pairing of meiotic chromosomes in the ciliate Tetrahymena thermophila. J. Cell Sci. 117:Part 245791–801 https://doi.org/10.1242/jcs.01504
    [Crossref] [Google Scholar]
  94. Long H, Doak TG, Lynch M. 2018. Limited mutation-rate variation within the Paramecium aurelia species complex. G3 8:72523–26 https://doi.org/10.1534/g3.118.200420
    [Crossref] [Google Scholar]
  95. Long H, Winter DJ, Chang AY-C, Sung W, Wu SH et al. 2016. Low base-substitution mutation rate in the germline genome of the ciliate Tetrahymena thermophil. Genome Biol. Evol. 8:123629–39 https://doi.org/10.1093/gbe/evw223
    [Crossref] [Google Scholar]
  96. Luo G-Z, Hao Z, Luo L, Shen M, Sparvoli D et al. 2018. N6-methyldeoxyadenosine directs nucleosome positioning in Tetrahymena DNA. Genome Biol 19:200 https://doi.org/10.1186/s13059-018-1573-3
    [Crossref] [Google Scholar]
  97. Luo Z, Hu T, Jiang H, Wang R, Q Xu et al. 2020. Rearrangement of macronucleus chromosomes correspond to TAD-like structures of micronucleus chromosomes in Tetrahymena thermophila. Genome Res 30:3406–14 https://doi.org/10.1101/gr.241687.118
    [Crossref] [Google Scholar]
  98. Luporini P, Pedrini B, Alimenti C, Vallesi A. 2016. Revisiting fifty years of research on pheromone signaling in ciliates. Eur. J. Protistol. 55:Part A26–38 https://doi.org/10.1016/j.ejop.2016.04.006
    [Crossref] [Google Scholar]
  99. Ma M, Stoyanova M, Rademacher G, Dutcher SK, Brown A, Zhang R. 2019. Structure of the decorated ciliary doublet microtubule. Cell 179:4909–22.e12 https://doi.org/10.1016/j.cell.2019.09.030
    [Crossref] [Google Scholar]
  100. Mali GR, Ali FA, Lau CK, Begum F, Boulanger J et al. 2021. Shulin packages axonemal outer dynein arms for ciliary targeting. Science 371:6532910–16 https://doi.org/10.1126/science.abe0526
    [Crossref] [Google Scholar]
  101. Marshall WF. 2019. Cellular cognition: sequential logic in a giant protist. Curr. Biol. 29:24R1303–5 https://doi.org/10.1016/j.cub.2019.10.034
    [Crossref] [Google Scholar]
  102. Marshall WF. 2020. Pattern formation and complexity in single cells. Curr. Biol. 30:10R544–52 https://doi.org/10.1016/j.cub.2020.04.011
    [Crossref] [Google Scholar]
  103. Marshall WF. 2021. Regeneration in Stentor coeruleus. Front. Cell Dev. Biol. 9:753625 https://doi.org/10.3389/fcell.2021.753625
    [Crossref] [Google Scholar]
  104. Maurer-Alcalá XX, Knight R, Katz LA. 2018a. Exploration of the germline genome of the ciliate Chilodonella uncinata through single-cell omics (transcriptomics and genomics). MBio 9:e01836 https://doi.org/10.1128/mBio.01836-17
    [Crossref] [Google Scholar]
  105. Maurer-Alcalá XX, Nowacki M 2019. Evolutionary origins and impacts of genome architecture in ciliates. Ann. N.Y. Acad. Sci. 1447:1110–18 https://doi.org/10.1111/nyas.14108
    [Crossref] [Google Scholar]
  106. Maurer-Alcalá XX, Yan Y, Pilling OA, Knight R, Katz LA. 2018b. Twisted tales: insights into genome diversity of ciliates using single-cell ‘omics. Genome Biol. Evol. 10:81927–39 https://doi.org/10.1093/gbe/evy133
    [Crossref] [Google Scholar]
  107. McGrath CL, Gout J-F, Doak TG, Yanagi A, Lynch M. 2014a. Insights into three whole-genome duplications gleaned from the Paramecium caudatum genome sequence. Genetics 197:41417–28 https://doi.org/10.1534/genetics.114.163287
    [Crossref] [Google Scholar]
  108. McGrath CL, Gout J-F, Johri P, Doak TG, Lynch M. 2014b. Differential retention and divergent resolution of duplicate genes following whole-genome duplication. Genome Res 24:101665–75 https://doi.org/10.1101/gr.173740.114
    [Crossref] [Google Scholar]
  109. Moriyama Y, Koshiba-Takeuchi K. 2018. Significance of whole-genome duplications on the emergence of evolutionary novelties. Brief. Funct. Genom. 17:5329–38 https://doi.org/10.1093/bfgp/ely007
    [Crossref] [Google Scholar]
  110. Mozzicafreddo M, Pucciarelli S, Swart EC, Piersanti A, Emmerich C et al. 2021. The macronuclear genome of the Antarctic psychrophilic marine ciliate Euplotes focardii reveals new insights on molecular cold adaptation. Sci. Rep. 11:18782 https://doi.org/10.1038/s41598-021-98168-5
    [Crossref] [Google Scholar]
  111. Nabeel-Shah S, Ashraf K, Saettone A, Garg J, Derynck J et al. 2020. Nucleus-specific linker histones Hho1 and Mlh1 form distinct protein interactions during growth, starvation and development in Tetrahymena thermophila. Sci. Rep. 10:168 https://doi.org/10.1038/s41598-019-56867-0
    [Crossref] [Google Scholar]
  112. Nabeel-Shah S, Garg J, Saettone A, Ashraf K, Lee H et al. 2021. Functional characterization of RebL1 highlights the evolutionary conservation of oncogenic activities of the RBBP4/7 orthologue in Tetrahymena thermophila. Nucleic Acids Res 49:116196–212 https://doi.org/10.1093/nar/gkab413
    [Crossref] [Google Scholar]
  113. Nabi A, Yano J, Valentine MS, Picariello T, Van Houten JL. 2019. SF-assemblin genes in Paramecium: phylogeny and phenotypes of RNAi silencing on the ciliary-striated rootlets and surface organization. Cilia 8:2 https://doi.org/10.1186/s13630-019-0062-y
    [Crossref] [Google Scholar]
  114. Nilsson JR 1979. Phagotrophy in Tetrahymena. Biochemistry and Physiology of Protozoa, Vol. 2 SH Hutner, A Lwoff 339–79 New York: Academic
    [Google Scholar]
  115. Nusblat AD, Bright LJ, Turkewitz AP. 2012. Conservation and innovation in Tetrahymena membrane traffic: proteins, lipids, and compartments. In Tetrahymena thermophila ed. K Collins pp. 14175 Methods Cell Biol. 109. Waltham, MA: Academic https://doi.org/10.1016/B978-0-12-385967-9.00006-2
    [Crossref] [Google Scholar]
  116. Onsbring H, Jamy M, Ettema TJG. 2018. RNA sequencing of Stentor cell fragments reveals transcriptional changes during cellular regeneration. Curr. Biol. 28:81281–88.e3 https://doi.org/10.1016/j.cub.2018.02.055
    [Crossref] [Google Scholar]
  117. Orias E, Singh DP, Meyer E 2017. Genetics and epigenetics of mating type determination in Paramecium and Tetrahymena. Annu. Rev. Microbiol. 71:133–56 https://doi.org/10.1146/annurev-micro-090816-093342
    [Crossref] [Google Scholar]
  118. Owa M, Uchihashi T, Yanagisawa H-A, Yamano T, Iguchi H et al. 2019. Inner lumen proteins stabilize doublet microtubules in cilia and flagella. Nat. Commun. 10:1143 https://doi.org/10.1038/s41467-019-09051-x
    [Crossref] [Google Scholar]
  119. Papazyan R, Voronina E, Chapman JR, Luperchio TR, Gilbert TM et al. 2014. Methylation of histone H3K23 blocks DNA damage in pericentric heterochromatin during meiosis. eLife 3:e02996 https://doi.org/10.7554/eLife.02996
    [Crossref] [Google Scholar]
  120. Park T, Wijeratne S, Meulia T, Firkins JL, Yu Z 2021. The macronuclear genome of anaerobic ciliate Entodinium caudatum reveals its biological features adapted to the distinct rumen environment. Genomics 113:31416–27 https://doi.org/10.1016/j.ygeno.2021.03.014
    [Crossref] [Google Scholar]
  121. Patel S, Docampo R. 2010. Acidic calcium stores open for business: expanding the potential for intracellular Ca2+ signaling. Trends Cell Biol 20:5277–86 https://doi.org/10.1016/J.TCB.2010.02.003
    [Crossref] [Google Scholar]
  122. Pedrini B, Finke AD, Marsh M, Luporini P, Vallesi A, Alimenti C. 2021. Crystal structure of the pheromone Er-13 from the ciliate Euplotes raikovi, with implications for a protein-protein association model in pheromone/receptor interactions. J. Struct. Biol. 214:1107812 https://doi.org/10.1016/j.jsb.2021.107812
    [Crossref] [Google Scholar]
  123. Pedrini B, Suter-Stahel T, Vallesi A, Alimenti C, Luporini P. 2017. Molecular structures and coding genes of the water-borne protein pheromones of Euplotes petzi, an early diverging polar species of Euplotes. J. Eukaryot. Microbiol. 64:2164–72 https://doi.org/10.1111/jeu.12348
    [Crossref] [Google Scholar]
  124. Pereira-Leal JB, Seabra MC. 2001. Evolution of the Rab family of small GTP-binding proteins. J. Mol. Biol. 313:4889–901 https://doi.org/10.1006/JMBI.2001.5072
    [Crossref] [Google Scholar]
  125. Phadke SS, Zufall RA. 2009. Rapid diversification of mating systems in ciliates. Biol. J. Linnean Soc. 98:1187–97 https://doi.org/10.1111/j.1095-8312.2009.01250.x
    [Crossref] [Google Scholar]
  126. Pillai AN, Shukla S, Gautam S, Rahaman A. 2017a. Small phosphatidate phosphatase (TtPAH2) of Tetrahymena complements respiratory function and not membrane biogenesis function of yeast PAH1. J. Biosci. 42:4613–21 https://doi.org/10.1007/s12038-017-9712-7
    [Crossref] [Google Scholar]
  127. Pillai AN, Shukla S, Rahaman A. 2017b. An evolutionarily conserved phosphatidate phosphatase maintains lipid droplet number and endoplasmic reticulum morphology but not nuclear morphology. Biol. Open 6:111629–43 https://doi.org/10.1242/bio.028233
    [Crossref] [Google Scholar]
  128. Plattner H. 2010. Membrane trafficking in protozoa SNARE proteins, H+-ATPase, actin, and other key players in ciliates. Int. Rev. Cell Mol. Biol. 280:79–184 https://doi.org/10.1016/S1937-6448(10)80003-6
    [Crossref] [Google Scholar]
  129. Plattner H. 2014. Calcium regulation in the protozoan model, Paramecium tetraurelia. J. Eukaryot. Microbiol. 61:195–114 https://doi.org/10.1111/JEU.12070
    [Crossref] [Google Scholar]
  130. Plattner H. 2015. The contractile vacuole complex of protists–new cues to function and biogenesis. Crit. Rev. Microbiol. 41:2218–27 https://doi.org/10.3109/1040841X.2013.821650
    [Crossref] [Google Scholar]
  131. Plattner H, Verkhratsky A. 2018. The remembrance of the things past: conserved signalling pathways link protozoa to mammalian nervous system. Cell Calcium 73:25–39 https://doi.org/10.1016/J.CECA.2018.04.001
    [Crossref] [Google Scholar]
  132. Preston RR. 1990. Genetic dissection of Ca2+-dependent ion channel function in Paramecium. BioEssays 12:6273–81 https://doi.org/10.1002/BIES.950120605
    [Crossref] [Google Scholar]
  133. Rahaman A, Elde NC, Turkewitz AP. 2008. A dynamin-related protein required for nuclear remodeling in Tetrahymena. Curr. Biol. 18:1227–33 https://doi.org/10.1016/j.cub.2008.07.042
    [Crossref] [Google Scholar]
  134. Reiter JF, Leroux MR. 2017. Genes and molecular pathways underpinning ciliopathies. Nat. Rev. Mol. Cell Biol. 18:9533–47 https://doi.org/10.1038/nrm.2017.60
    [Crossref] [Google Scholar]
  135. Ricard G, de Graaf RM, Dutilh BE, Duarte I, van Alen TA et al. 2008. Macronuclear genome structure of the ciliate Nyctotherus ovalis: single-gene chromosomes and tiny introns. BMC Genom. 9:587 https://doi.org/10.1186/1471-2164-9-587
    [Crossref] [Google Scholar]
  136. Ruehle MD, Orias E, Pearson CG. 2016. Tetrahymena as a unicellular model eukaryote: genetic and genomic tools. Genetics 203:2649–65 https://doi.org/10.1534/genetics.114.169748
    [Crossref] [Google Scholar]
  137. Ruehle MD, Stemm-Wolf AJ, Pearson CG. 2020. Sas4 links basal bodies to cell division via Hippo signaling. J. Cell Biol. 219:8e201906183 https://doi.org/10.1083/jcb.201906183
    [Crossref] [Google Scholar]
  138. Rzeszutek I, Maurer-Alcalá XX, Nowacki M 2020. Programmed genome rearrangements in ciliates. Cell. Mol. Life Sci. 77:224615–29 https://doi.org/10.1007/s00018-020-03555-2
    [Crossref] [Google Scholar]
  139. Saettone A, Nabeel-Shah S, Garg J, Lambert J-P, Pearlman RE, Fillingham J. 2019. Functional proteomics of nuclear proteins in Tetrahymena thermophila: a review. Genes 10:5E333 https://doi.org/10.3390/genes10050333
    [Crossref] [Google Scholar]
  140. Saibil HR. 2022. Cryo-EM in molecular and cellular biology. Mol. Cell 82:2274–84 https://doi.org/10.1016/j.molcel.2021.12.016
    [Crossref] [Google Scholar]
  141. Saito-Nakano Y, Nakahara T, Nakano K, Nozaki T, Numata O. 2010. marked amplification and diversification of products of Ras genes from rat brain, Rab GTPases, in the ciliates Tetrahymena thermophila and Paramecium tetraurelia. J. Eukaryot. Microbiol. 57:5389–99 https://doi.org/10.1111/j.1550-7408.2010.00503.x
    [Crossref] [Google Scholar]
  142. Sawka-Gądek N, Potekhin A, Singh DP, Grevtseva I, Arnaiz O et al. 2021. Evolutionary plasticity of mating-type determination mechanisms in Paramecium aurelia sibling species. Genome Biol. Evol. 13:2evaa258 https://doi.org/10.1093/gbe/evaa258
    [Crossref] [Google Scholar]
  143. Sellis D, Guérin F, Arnaiz O, Pett W, Lerat E et al. 2021. Massive colonization of protein-coding exons by selfish genetic elements in Paramecium germline genomes. PLOS Biol 19:7e3001309 https://doi.org/10.1371/journal.pbio.3001309
    [Crossref] [Google Scholar]
  144. Shukla S, Pillai AN, Rahaman A. 2018. A putative NEM1 homologue regulates lipid droplet biogenesis via PAH1 in Tetrahymena thermophila. J. Biosci. 43:4693–706
    [Google Scholar]
  145. Singh DP, Saudemont B, Guglielmi G, Arnaiz O, J-F Goût et al. 2014. Genome-defence small RNAs exapted for epigenetic mating-type inheritance. Nature 509:7501447–52 https://doi.org/10.1038/nature13318
    [Crossref] [Google Scholar]
  146. Slabodnick MM, Ruby JG, Dunn JG, Feldman JL, DeRisi JL, Marshall WF. 2014. The kinase regulator Mob1 acts as a patterning protein for Stentor morphogenesis. PLOS Biol 12:5e1001861 https://doi.org/10.1371/journal.pbio.1001861
    [Crossref] [Google Scholar]
  147. Slabodnick MM, Ruby JG, Reiff SB, Swart EC, Gosai S et al. 2017. The macronuclear genome of Stentor coeruleus reveals tiny introns in a giant cell. Curr. Biol. 27:4569–75 https://doi.org/10.1016/j.cub.2016.12.057
    [Crossref] [Google Scholar]
  148. Smith DGS, Gawryluk RMR, Spencer DF, Pearlman RE, Siu KWM, Gray MW. 2007. Exploring the mitochondrial proteome of the ciliate protozoon Tetrahymena thermophila: direct analysis by tandem mass spectrometry. J. Mol. Biol. 374:3837–63 https://doi.org/10.1016/j.jmb.2007.09.051
    [Crossref] [Google Scholar]
  149. Smith S, Maurer-Alcalá X, Yan Y, Katz L, Santoferrara L, McManus G. 2020. Combined genome and transcriptome analyses of the ciliate Schmidingerella arcuata (Spirotrichea) reveal patterns of DNA elimination, scrambling, and inversion. Genome Biol. Evol. 12:91616–22 https://doi.org/10.1093/gbe/evaa185
    [Crossref] [Google Scholar]
  150. Soh AWJ, Pearson CG. 2021. Ciliate cortical organization and dynamics for cell motility: comparing ciliates and vertebrates. J. Eukaryot. Microbiol. 00:e12880 https://doi.org/10.1111/jeu.12880
    [Crossref] [Google Scholar]
  151. Soh AWJ, van Dam TJP, Stemm-Wolf AJ, Pham AT, Morgan GP et al. 2020. Ciliary force-responsive striated fibers promote basal body connections and cortical interactions. J. Cell Biol. 219:1e201904091 https://doi.org/10.1083/jcb.201904091
    [Crossref] [Google Scholar]
  152. Sonneborn TM. 1977. Local differentiation of the cell surface of ciliates: their determination, effects and genetics. The Synthesis, Assembly and Turnover of Cell Surface Components, ed. G Poste, GL Nicolson 829–56 Amsterdam: North Holland Pub.
    [Google Scholar]
  153. Spang A. 2016. Membrane tethering complexes in the endosomal system. Front. Cell Dev. Biol. 4:35 https://doi.org/10.3389/FCELL.2016.00035
    [Crossref] [Google Scholar]
  154. Sparvoli D, Richardson E, Osakada H, Lan X, Iwamoto M et al. 2018. Remodeling the specificity of an endosomal CORVET tether underlies formation of regulated secretory vesicles in the ciliate Tetrahymena thermophila. Curr. Biol. 28:5697–710.e13 https://doi.org/10.1016/j.cub.2018.01.047
    [Crossref] [Google Scholar]
  155. Sparvoli D, Zoltner M, Cheng CY, Field MC, Turkewitz AP. 2020. Diversification of CORVET tethers facilitates transport complexity in Tetrahymena thermophila. J. Cell Sci. 133:3jcs238659 https://doi.org/10.1242/jcs.238659
    [Crossref] [Google Scholar]
  156. Stenmark H. 2009. Rab GTPases as coordinators of vesicle traffic. Nat. Rev. Mol. Cell Biol. 10:8513–25 https://doi.org/10.1038/nrm2728
    [Crossref] [Google Scholar]
  157. Stoddard D, Zhao Y, Bayless BA, Gui L, Louka P et al. 2018. Tetrahymena RIB72A and RIB72B are microtubule inner proteins in the ciliary doublet microtubules. Mol. Biol. Cell 29:212566–77 https://doi.org/10.1091/mbc.E18-06-0405
    [Crossref] [Google Scholar]
  158. Stover NA, Punia RS, Bowen MS, Dolins SB, Clark TG. 2012. Tetrahymena genome database Wiki: a community-maintained model organism database. Database 2012:bas007 https://doi.org/10.1093/database/bas007
    [Crossref] [Google Scholar]
  159. Stuart KR, Cole ES. 2000. Nuclear and cytoskeletal fluorescence microscopy techniques. In Tetrahymena thermophila ed. DJ Asai, JD Forney pp. 291311 Methods Cell Biol. 62. San Diego, CA: Academic https://doi.org/10.1016/s0091-679x(08)61538-1
    [Crossref] [Google Scholar]
  160. Su Z, Zhang K, Kappel K, S Li, Palo MZ et al. 2021. Cryo-EM structures of full-length Tetrahymena ribozyme at 3.1 Å resolution. Nature 596:7873603–7 https://doi.org/10.1038/s41586-021-03803-w
    [Crossref] [Google Scholar]
  161. Sugiura M, Yuasa HJ, Harumoto T. 2017. Novel specificity of IDO enzyme involved in the biosynthesis of mating pheromone in the ciliate Blepharisma stoltei. Protist 168:6686–96 https://doi.org/10.1016/j.protis.2017.09.003
    [Crossref] [Google Scholar]
  162. Suhren JH, Noto T, Kataoka K, Gao S, Liu Y, Mochizuki K. 2017. Negative regulators of an RNAi-heterochromatin positive feedback loop safeguard somatic genome integrity in Tetrahymena. Cell Rep 18:102494–507 https://doi.org/10.1016/j.celrep.2017.02.024
    [Crossref] [Google Scholar]
  163. Swart EC, Bracht JR, Magrini V, Minx P, Chen X et al. 2013. The Oxytricha trifallax macronuclear genome: a complex eukaryotic genome with 16,000 tiny chromosomes. PLOS Biol 11:1e1001473 https://doi.org/10.1371/journal.pbio.1001473
    [Crossref] [Google Scholar]
  164. Swart EC, Serra V, Petroni G, Nowacki M. 2016. Genetic codes with no dedicated stop codon: context-dependent translation termination. Cell 166:3691–702 https://doi.org/10.1016/j.cell.2016.06.020
    [Crossref] [Google Scholar]
  165. Takahashi M, Naitoh Y. 1978. Behavioural mutants of Paramecium caudatum with defective membrane electrogenesis. Nature 271:5646656–59 https://doi.org/10.1038/271656a0
    [Crossref] [Google Scholar]
  166. Tartar V. 1968. Micrurgical experiments on cytokinesis in Stentor coeruleus. J. Exp. Zool. 167:121–36 https://doi.org/10.1002/jez.1401670103
    [Crossref] [Google Scholar]
  167. Taylor CW, Da Fonseca PCA, Morris EP 2004. IP3 receptors: the search for structure. Trends Biochem. Sci. 29:4210–19 https://doi.org/10.1016/J.TIBS.2004.02.010
    [Crossref] [Google Scholar]
  168. Tobiasson V, Amunts A. 2020. Ciliate mitoribosome illuminates evolutionary steps of mitochondrial translation. eLife 9:e59264 https://doi.org/10.7554/eLife.59264
    [Crossref] [Google Scholar]
  169. Urbanska P, Joachimiak E, Bazan R, Fu G, Poprzeczko M et al. 2018. Ciliary proteins Fap43 and Fap44 interact with each other and are essential for proper cilia and flagella beating. Cell. Mol. Life Sci. 75:244479–93 https://doi.org/10.1007/s00018-018-2819-7
    [Crossref] [Google Scholar]
  170. Uspenskaya ZI, Yudin AL. 2016. Fifty years of research on serotypes and mating types in Dileptus anser: a review. Eur. J. Protistol. 53:31–44 https://doi.org/10.1016/j.ejop.2015.12.004
    [Crossref] [Google Scholar]
  171. Valentine MS, Van Houten J. 2022. Ion channels of cilia: Paramecium as a model. J. Eukaryot. Microbiol. 00:e12884 https://doi.org/10.1111/JEU.12884
    [Crossref] [Google Scholar]
  172. van der Beek J, Jonker C, van der Welle R, Liv N, Klumperman J. 2019. CORVET, CHEVI and HOPS – multisubunit tethers of the endo-lysosomal system in health and disease. J. Cell Sci. 132:10jcs189134 https://doi.org/10.1242/jcs.189134
    [Crossref] [Google Scholar]
  173. Van Houten J. 2019. Paramecium biology. Results Probl. . Cell Differ. 68:291–318 https://doi.org/10.1007/978-3-030-23459-1_13
    [Crossref] [Google Scholar]
  174. Vinogradov DV, Tsoi˘ OV, Zaika AV, Lobanov AV, Turanov AA et al. 2012. [Draft macronuclear genome of a ciliate Euplotes crassus]. Mol. Biol. 46:2361–66 (In Russian)
    [Google Scholar]
  175. Wahab S, Saettone A, Nabeel-Shah S, Dannah N, Fillingham J. 2020. Exploring the histone acetylation cycle in the protozoan model Tetrahymena thermophila. Front. Cell Dev. Biol. 8:509 https://doi.org/10.3389/fcell.2020.00509
    [Crossref] [Google Scholar]
  176. Wang G, Chen K, Zhang J, Deng S, Xiong J et al. 2020. Drivers of mating type composition in Tetrahymena thermophila. Genome Biol. Evol. 12:122328–43 https://doi.org/10.1093/gbe/evaa197
    [Crossref] [Google Scholar]
  177. Wang R-L, Miao W, Wang W, Xiong J, Liang A-H. 2018. EOGD: the Euplotes octocarinatus genome database. BMC Genom 19:63 https://doi.org/10.1186/s12864-018-4445-z
    [Crossref] [Google Scholar]
  178. Wang Y, Wang YY, Sheng Y, Huang J, Chen X et al. 2017. A comparative study of genome organization and epigenetic mechanisms in model ciliates, with an emphasis on Tetrahymena, Paramecium and Oxytricha. Eur. J. Protistol. 61:Part B376–87 https://doi.org/10.1016/j.ejop.2017.06.006
    [Crossref] [Google Scholar]
  179. Wang YY, Sheng Y, Liu Y, Pan B, Huang J et al. 2017. N6-methyladenine DNA modification in the unicellular eukaryotic organism Tetrahymena thermophila. Eur. J. Protistol. 58:94–102 https://doi.org/10.1016/j.ejop.2016.12.003
    [Crossref] [Google Scholar]
  180. Wang YY, Sheng Y, Liu Y, Zhang W, Cheng T et al. 2019. A distinct class of eukaryotic MT-A70 methyltransferases maintain symmetric DNA N6-adenine methylation at the ApT dinucleotides as an epigenetic mark associated with transcription. Nucleic Acids Res 47:2211771–89 https://doi.org/10.1093/nar/gkz1053
    [Crossref] [Google Scholar]
  181. Warren A, Patterson DJ, Dunthorn M, Clamp JC, Achilles-Day UEM et al. 2017. Beyond the ‘code’: a guide to the description and documentation of biodiversity in ciliated protists (Alveolata, Ciliophora). J. Eukaryot. Microbiol. 64:4539–54 https://doi.org/10.1111/jeu.12391
    [Crossref] [Google Scholar]
  182. Wloga D, Frankel J. 2012. From molecules to morphology: cellular organization of Tetrahymena thermophila. In Tetrahymena thermophila ed. K Collins pp. 83140 Methods Cell Biol. 109. Waltham, MA: Academic https://doi.org/10.1016/B978-0-12-385967-9.00005-0
    [Crossref] [Google Scholar]
  183. Xiong J, Lu Y, Feng J, Yuan D, Tian M et al. 2013. Tetrahymena functional genomics database (TetraFGD): an integrated resource for Tetrahymena functional genomics. Database 2013:bat008 https://doi.org/10.1093/database/bat008
    [Crossref] [Google Scholar]
  184. Xiong J, Yang W, Chen K, Jiang C, Ma Y et al. 2019. Hidden genomic evolution in a morphospecies – the landscape of rapidly evolving genes in Tetrahymena. PLOS Biol 17:6e3000294 https://doi.org/10.1371/journal.pbio.3000294
    [Crossref] [Google Scholar]
  185. Xu J, Zhao X, Mao F, Basrur V, Ueberheide B et al. 2021. A Polycomb repressive complex is required for RNAi-mediated heterochromatin formation and dynamic distribution of nuclear bodies. Nucleic Acids Res 49:105407–25 https://doi.org/10.1093/nar/gkaa1262
    [Crossref] [Google Scholar]
  186. Xu K, Doak TG, Lipps HJ, Wang J, Swart EC, Chang W-J. 2012. Copy number variations of 11 macronuclear chromosomes and their gene expression in Oxytricha trifallax. Gene 505:175–80 https://doi.org/10.1016/j.gene.2012.05.045
    [Crossref] [Google Scholar]
  187. Yan G, Yang W, Han X, Chen K, Xiong J et al. 2020. Evolution of the mating type gene pair and multiple sexes in Tetrahymena. iScience 24:101950 https://doi.org/10.1016/j.isci.2020.101950
    [Crossref] [Google Scholar]
  188. Yan Y, Maurer-Alcalá XX, Knight R, Pond SLK, Katz LA. 2019. Single-cell transcriptomics reveal a correlation between genome architecture and gene family evolution in ciliates. MBio 10:6e02524 https://doi.org/10.1128/mBio.02524-19
    [Crossref] [Google Scholar]
  189. Yuasa HJ, Sugiura M, Harumoto T. 2018. A single amino acid residue regulates the substrate affinity and specificity of indoleamine 2,3-dioxygenase. Arch. Biochem. Biophys. 640:1–9 https://doi.org/10.1016/j.abb.2017.12.019
    [Crossref] [Google Scholar]
  190. Zhang KS, Blauch LR, Huang W, Marshall WF, Tang SKY. 2021. Microfluidic guillotine reveals multiple timescales and mechanical modes of wound response in Stentor coeruleus. BMC Biol 19:63 https://doi.org/10.1186/s12915-021-00970-0
    [Crossref] [Google Scholar]
  191. Zheng W, Wang C, Lynch M, Gao S. 2021. The compact macronuclear genome of the ciliate Halteria grandinella: a transcriptome-like genome with 23,000 nanochromosomes. MBio 12:e01964–20 https://doi.org/10.1128/mBio.01964-20
    [Crossref] [Google Scholar]
  192. Zheng W, Wang C, Yan Y, Gao F, Doak TG, Song W. 2018. Insights into an extensively fragmented eukaryotic genome: de novo genome sequencing of the multinuclear ciliate Uroleptopsis citrina. Genome Biol. Evol. 10:3883–94 https://doi.org/10.1093/gbe/evy055
    [Crossref] [Google Scholar]
/content/journals/10.1146/annurev-cellbio-120420-020656
Loading
/content/journals/10.1146/annurev-cellbio-120420-020656
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error