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Abstract

The extent of intraspecific genomic variation is key to understanding species evolutionary history, including recent adaptive shifts. Intraspecific genomic variation remains poorly explored in eukaryotic micro-organisms, especially in the nuclear dimorphic ciliates, despite their fundamental role as laboratory model systems and their ecological importance in many ecosystems. We sequenced the macronuclear genome of 22 laboratory strains of the oligohymenophoran , a model species in both cellular biology and evolutionary ecology. We explored polymorphisms at the junctions of programmed eliminated sequences, and reveal their utility to barcode very closely related cells. As for other species of the genus , we confirm micronuclear centromeres as gene diversification centres in , but also reveal a two-speed evolution in these regions. In the rest of the genome, we highlight recent diversification of genes coding for extracellular proteins and cell adhesion. We discuss all these findings in relation to this ciliate’s ecology and cellular characteristics.

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2024-01-11
2025-02-17
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References

  1. Hendry AP. Eco-Evolutionary Dynamics Princeton and Oxford: Princeton University Press; 2016 [View Article]
    [Google Scholar]
  2. Darwin C. On the Origin of Species London: John Murray;
    [Google Scholar]
  3. Reva B, Antipin Y, Sander C. Predicting the functional impact of protein mutations: application to cancer genomics. Nucleic Acids Res 2011; 39:e118 [View Article] [PubMed]
    [Google Scholar]
  4. Collins K, Gorovsky MA. Tetrahymena thermophila. Curr Biol 2005; 15:R317–8 [View Article] [PubMed]
    [Google Scholar]
  5. Ruehle MD, Orias E, Pearson CG. Tetrahymena as a unicellular model eukaryote: genetic and genomic tools. Genetics 2016; 203:649–665 [View Article] [PubMed]
    [Google Scholar]
  6. Kataoka K, Mochizuki K. Programmed DNA elimination in Tetrahymena: a small RNA-mediated genome surveillance mechanism. Adv Exp Med Biol 2011; 722:156–173 [View Article] [PubMed]
    [Google Scholar]
  7. Jiang Y-Y, Maier W, Baumeister R, Minevich G, Joachimiak E et al. The hippo pathway maintains the equatorial division plane in the ciliate Tetrahymena. Genetics 2017; 206:873–888 [View Article] [PubMed]
    [Google Scholar]
  8. Kushida Y, Nakano K, Numata O. Amitosis requires γ-tubulin-mediated microtubule assembly in Tetrahymena thermophila. Cytoskeleton 2011; 68:89–96 [View Article] [PubMed]
    [Google Scholar]
  9. Altermatt F, Fronhofer EA, Garnier A, Giometto A, Hammes F et al. Big answers from small worlds: a user’s guide for protist microcosms as a model system in ecology and evolution. Methods Ecol Evol 2015; 6:218–231 [View Article]
    [Google Scholar]
  10. Collins K. Tetrahymena Thermophila Elsevier: Academic Press; 2012
    [Google Scholar]
  11. Junker AD, Jacob S, Philippe H, Legrand D, Pearson CG. Plastic cell morphology changes during dispersal. iScience 2021; 24:102915 [View Article] [PubMed]
    [Google Scholar]
  12. Nelsen EM, Debault LE. Transformation in Tetrahymena pyriformis: description of an inducible phenotype. J Protozool 1978; 25:113–119 [View Article] [PubMed]
    [Google Scholar]
  13. Fronhofer EA, Altermatt F. Eco-evolutionary feedbacks during experimental range expansions. Nat Commun 2015; 6:6844 [View Article] [PubMed]
    [Google Scholar]
  14. Morel‐Journel T, Thuillier V, Pennekamp F, Laurent E, Legrand D et al. A multidimensional approach to the expression of phenotypic plasticity. Funct Ecol 2020; 34:2338–2349 [View Article]
    [Google Scholar]
  15. Schtickzelle N, Fjerdingstad EJ, Chaine A, Clobert J. Cooperative social clusters are not destroyed by dispersal in a ciliate. BMC Evol Biol 2009; 9:251 [View Article] [PubMed]
    [Google Scholar]
  16. Jacob S, Legrand D, Chaine AS, Bonte D, Schtickzelle N et al. Gene flow favours local adaptation under habitat choice in ciliate microcosms. Nat Ecol Evol 2017; 1:1407–1410 [View Article]
    [Google Scholar]
  17. Chaine AS, Schtickzelle N, Polard T, Huet M, Clobert J. Kin-Based recognition and social aggregation in a ciliate. Evolution 2010; 64:1290–1300 [View Article] [PubMed]
    [Google Scholar]
  18. Friman V-P, Jousset A, Buckling A. Rapid prey evolution can alter the structure of predator-prey communities. J Evol Biol 2014; 27:374–380 [View Article] [PubMed]
    [Google Scholar]
  19. Aijaz I, Koudelka GB. Tetrahymena phagocytic vesicles as ecological micro-niches of phage transfer. FEMS Microbiol Ecol 2017; 93: [View Article] [PubMed]
    [Google Scholar]
  20. Somasundaram S, Abraham JS, Maurya S, Makhija S, Gupta R et al. Cellular and molecular basis of heavy metal-induced stress in ciliates. Curr Sci 2018; 114:1858 [View Article]
    [Google Scholar]
  21. Chen F, Leick V. The protozoan Tetrahymena as a bioindicator to screen bioactive substances. J Microbiol Methods 2004; 59:233–241 [View Article] [PubMed]
    [Google Scholar]
  22. Hamilton EP, Kapusta A, Huvos PE, Bidwell SL, Zafar N et al. Structure of the germline genome of Tetrahymena thermophila and relationship to the massively rearranged somatic genome. Elife 2016; 5:e19090 [View Article] [PubMed]
    [Google Scholar]
  23. Eisen JA, Coyne RS, Wu M, Wu D, Thiagarajan M et al. Macronuclear genome sequence of the ciliate Tetrahymena thermophila, a model eukaryote. PLoS Biol 2006; 4:e286 [View Article]
    [Google Scholar]
  24. Sheng Y, Duan L, Cheng T, Qiao Y, Stover NA et al. The completed macronuclear genome of a model ciliate Tetrahymena thermophila and its application in genome scrambling and copy number analyses. Sci China Life Sci 2020; 63:1534–1542 [View Article] [PubMed]
    [Google Scholar]
  25. Rzeszutek I, Maurer-Alcalá XX, Nowacki M. Programmed genome rearrangements in ciliates. Cell Mol Life Sci 2020; 77:4615–4629 [View Article]
    [Google Scholar]
  26. Zhou Y, Fu L, Mochizuki K, Xiong J, Miao W et al. Absolute quantification of chromosome copy numbers in the polyploid macronucleus of Tetrahymena thermophila at the single-cell level. J Eukaryot Microbiol 2022; 69:e12907 [View Article] [PubMed]
    [Google Scholar]
  27. Prescott DM. The DNA of ciliated protozoa. Microbiol Rev 1994; 58:233–267 [View Article] [PubMed]
    [Google Scholar]
  28. Spring KJ, Pham S, Zufall RA. Chromosome copy number variation and control in the ciliate Chilodonella uncinata. PLoS One 2013; 8:e56413 [View Article] [PubMed]
    [Google Scholar]
  29. Cheng Y-H, Liu C-FJ, Yu Y-H, Jhou Y-T, Fujishima M et al. Genome plasticity in Paramecium bursaria revealed by population genomics. BMC Biol 2020; 18:180 [View Article] [PubMed]
    [Google Scholar]
  30. Verdonck R, Legrand D, Jacob S, Philippe H. Phenotypic plasticity through disposable genetic adaptation in ciliates. Trends Microbiol 2022; 30:120–130 [View Article] [PubMed]
    [Google Scholar]
  31. de Francisco P, Martín-González A, Turkewitz AP, Gutiérrez JC. Genome plasticity in response to stress in Tetrahymena thermophila: selective and reversible chromosome amplification and paralogous expansion of metallothionein genes. Environ Microbiol 2018; 20:2410–2421 [View Article] [PubMed]
    [Google Scholar]
  32. Chalker DL, Yao M-C. DNA elimination in ciliates: transposon domestication and genome surveillance. Annu Rev Genet 2011; 45:227–246 [View Article] [PubMed]
    [Google Scholar]
  33. Drotos KHI, Zagoskin MV, Kess T, Gregory TR, Wyngaard GA. Throwing away DNA: programmed downsizing in somatic nuclei. Trends Genet 2022; 38:483–500 [View Article] [PubMed]
    [Google Scholar]
  34. Vogt A, Goldman AD, Mochizuki K, Landweber LF, Rosenberg SM. Transposon domestication versus mutualism in ciliate genome rearrangements. PLoS Genet 2013; 9:e1003659 [View Article]
    [Google Scholar]
  35. Xiong J, Yang W, Chen K, Jiang C, Ma Y et al. Hidden genomic evolution in a morphospecies-The landscape of rapidly evolving genes in Tetrahymena. PLoS Biol 2019; 17:e3000294 [View Article] [PubMed]
    [Google Scholar]
  36. Johri P, Krenek S, Marinov GK, Doak TG, Berendonk TU et al. Population genomics of Paramecium species. Mol Biol Evol 2017; 34:1194–1216 [View Article] [PubMed]
    [Google Scholar]
  37. Swart EC, Bracht JR, Magrini V, Minx P, Chen X et al. The Oxytricha trifallax macronuclear genome: a complex eukaryotic genome with 16,000 tiny chromosomes. PLoS Biol 2013; 11:e1001473 [View Article]
    [Google Scholar]
  38. Slabodnick MM, Ruby JG, Reiff SB, Swart EC, Gosai S et al. The macronuclear genome of stentor coeruleus reveals tiny introns in a giant cell. Curr Biol 2017; 27:569–575 [View Article] [PubMed]
    [Google Scholar]
  39. Jacob S, Chaine AS, Huet M, Clobert J, Legrand D. Variability in dispersal syndromes is a key driver of metapopulation dynamics in experimental microcosms. Am Nat 2019; 194:613–626 [View Article] [PubMed]
    [Google Scholar]
  40. Jacob S, Laurent E, Haegeman B, Bertrand R, Prunier JG et al. Habitat choice meets thermal specialization: competition with specialists may drive suboptimal habitat preferences in generalists. Proc Natl Acad Sci U S A 2018; 115:11988–11993 [View Article] [PubMed]
    [Google Scholar]
  41. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article] [PubMed]
    [Google Scholar]
  42. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article] [PubMed]
    [Google Scholar]
  43. Haubold B, Klötzl F, Pfaffelhuber P. andi: fast and accurate estimation of evolutionary distances between closely related genomes. Bioinformatics 2015; 31:1169–1175 [View Article] [PubMed]
    [Google Scholar]
  44. Wheeler TJ. Large-scale neighbor-joining with NINJA. In Salzberg SL, Warnow T. eds Proceedings of the 9th Workshop on Algorithms in Bioinformatics Berlin: Springer; 2009 pp 375–389 [View Article]
    [Google Scholar]
  45. Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One 2014; 9:e112963 [View Article] [PubMed]
    [Google Scholar]
  46. Li H, Durbin R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 2009; 25:1754–1760 [View Article]
    [Google Scholar]
  47. Danecek P, Bonfield JK, Liddle J, Marshall J, Ohan V et al. Twelve years of SAMtools and BCFtools. GigaScience 2021; 10: [View Article]
    [Google Scholar]
  48. Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 2010; 26:841–842 [View Article] [PubMed]
    [Google Scholar]
  49. Pitts RA, Doerder FP. Genomic exclusion and other micronuclear anomalies are common in genetically defective clones of Tetrahymena thermophila. Genetics 1988; 120:135–143 [View Article]
    [Google Scholar]
  50. Loidl J. Tetrahymena meiosis: simple yet ingenious. PLoS Genet 2021; 17:e1009627 [View Article] [PubMed]
    [Google Scholar]
  51. Begun DJ, Holloway AK, Stevens K, Hillier LW, Poh Y-P et al. Population genomics: whole-genome analysis of polymorphism and divergence in Drosophila simulans. PLoS Biol 2007; 5:e310 [View Article] [PubMed]
    [Google Scholar]
  52. Nei M, Gojobori T. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 1986; 3:418–426 [View Article] [PubMed]
    [Google Scholar]
  53. Stoletzki N, Eyre-Walker A. Estimation of the neutrality index. Mol Biol Evol 2011; 28:63–70 [View Article] [PubMed]
    [Google Scholar]
  54. Carbon S, Douglass E, Good BM, Unni DR. Gene Ontology Consortium The gene ontology resource: enriching a GOld mine. Nucleic Acids Res 2021; 49:D325–D334 [View Article] [PubMed]
    [Google Scholar]
  55. Reimand J, Kull M, Peterson H, Hansen J, Vilo J. g:Profiler--a web-based toolset for functional profiling of gene lists from large-scale experiments. Nucleic Acids Res 2007; 35:W193–200 [View Article] [PubMed]
    [Google Scholar]
  56. Doerder FP. Barcodes reveal 48 new species of Tetrahymena, Dexiostoma, and Glaucoma: phylogeny, ecology, and biogeography of new and established species. J Eukaryot Microbiol 2019; 66:182–208 [View Article] [PubMed]
    [Google Scholar]
  57. Brunk CF, Lee LC, Tran AB, Li J. Complete sequence of the mitochondrial genome of Tetrahymena thermophila and comparative methods for identifying highly divergent genes. Nucleic Acids Res 2003; 31:1673–1682 [View Article] [PubMed]
    [Google Scholar]
  58. Kobayashi T, Endoh H. Unusual distribution of mitochondrial large subunit rRNA in the cytosol during conjugation in Tetrahymena thermophila. Genes Genet Syst 2004; 79:255–262 [View Article] [PubMed]
    [Google Scholar]
  59. Lin C-Y, Chao J-L, Tsai H-K, Chalker D, Yao M-C. Setting boundaries for genome-wide heterochromatic DNA deletions through flanking inverted repeats in Tetrahymena thermophila. Nucleic Acids Res 2019; 47:5181–5192 [View Article]
    [Google Scholar]
  60. Doerder FP. Abandoning sex: multiple origins of asexuality in the ciliate Tetrahymena. BMC Evol Biol 2014; 14:112 [View Article] [PubMed]
    [Google Scholar]
  61. Wang G, Fu L, Xiong J, Mochizuki K, Fu Y et al. Identification and characterization of base-substitution mutations in the macronuclear genome of the ciliate Tetrahymena thermophila. Genome Biol Evol 2021; 13:evaa232 [View Article] [PubMed]
    [Google Scholar]
  62. Doerder FP, Gates MA, Eberhardt FP, Arslanyolu M. High frequency of sex and equal frequencies of mating types in natural populations of the ciliate Tetrahymena thermophila. Proc Natl Acad Sci U S A 1995; 92:8715–8718 [View Article] [PubMed]
    [Google Scholar]
  63. Zufall RA, Dimond KL, Doerder FP. Restricted distribution and limited gene flow in the model ciliate Tetrahymena thermophila. Mol Ecol 2013; 22:1081–1091 [View Article] [PubMed]
    [Google Scholar]
  64. Cayuela H, Rougemont Q, Prunier JG, Moore J-S, Clobert J et al. Demographic and genetic approaches to study dispersal in wild animal populations: a methodological review. Mol Ecol 2018; 27:3976–4010 [View Article] [PubMed]
    [Google Scholar]
  65. Jacob S, Legrand D. Phenotypic plasticity can reverse the relative extent of intra- and interspecific variability across a thermal gradient. Proc Biol Sci 2021; 288:20210428 [View Article] [PubMed]
    [Google Scholar]
  66. Long H, Winter DJ, Chang AY-C, Sung W, Wu SH et al. Low base-substitution mutation rate in the germline genome of the ciliate Tetrahymena thermophila. Evol Biol 2015 [View Article]
    [Google Scholar]
  67. Katju V, Bergthorsson U. Old trade, new tricks: insights into the spontaneous mutation process from the partnering of classical mutation accumulation experiments with high-throughput genomic approaches. Genome Biol Evol 2019; 11:136–165 [View Article] [PubMed]
    [Google Scholar]
  68. Xiong J, Lu X, Zhou Z, Chang Y, Yuan D et al. Transcriptome analysis of the model protozoan, Tetrahymena thermophila, using Deep RNA sequencing. PLoS ONE 2012; 7:e30630 [View Article] [PubMed]
    [Google Scholar]
  69. Simon EM, Nanney DL, Doerder FP. The “Tetrahymena pyriformis” complex of cryptic species. Biodivers Conserv 2008; 17:365–380 [View Article]
    [Google Scholar]
  70. Doerder FP, Brunk C. Natural populations and inbred strains of Tetrahymena. Methods Cell Biol 2012; 109:277–300 [View Article]
    [Google Scholar]
  71. Christensen ST, Rasmussen L. Evidence for growth factors which control cell multiplication in Tetrahymena thermophila. Acta Protozool 1992; 31:215–219
    [Google Scholar]
  72. Henikoff S, Ahmad K, Malik HS. The centromere paradox: stable inheritance with rapidly evolving DNA. Science 2001; 293:1098–1102 [View Article]
    [Google Scholar]
  73. Elde NC, Roach KC, Yao M-C, Malik HS. Absence of positive selection on centromeric histones in Tetrahymena suggests unsuppressed centromere: drive in lineages lacking male meiosis. J Mol Evol 2011; 72:510–520 [View Article] [PubMed]
    [Google Scholar]
  74. Zhao P, Malik S. The phosphorylation to acetylation/methylation cascade in transcriptional regulation: how kinases regulate transcriptional activities of DNA/histone-modifying enzymes. Cell Biosci 2022; 12:83 [View Article]
    [Google Scholar]
  75. Miao W, Xiong J, Bowen J, Wang W, Liu Y et al. Microarray analyses of gene expression during the Tetrahymena thermophila life cycle. PLoS ONE 2009; 4:e4429 [View Article] [PubMed]
    [Google Scholar]
  76. Austerberry CF, Allis CD, Yao MC. Specific DNA rearrangements in synchronously developing nuclei of Tetrahymena. Proc Natl Acad Sci U S A 1984; 81:7383–7387 [View Article] [PubMed]
    [Google Scholar]
  77. Noto T, Mochizuki K. Whats, hows and whys of programmed DNA elimination in Tetrahymena. Open Biol 2017; 7:170172 [View Article] [PubMed]
    [Google Scholar]
  78. Yin L, Gater ST, Karrer KM. A developmentally regulated gene, ASI2, is required for endocycling in the macronuclear anlagen of Tetrahymena. Eukaryot Cell 2010; 9:1343–1353 [View Article] [PubMed]
    [Google Scholar]
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