Section: Genomics
Topic: Genetics/Genomics, Evolution

Karyorelict ciliates use an ambiguous genetic code with context-dependent stop/sense codons

10.24072/pcjournal.141 - Peer Community Journal, Volume 2 (2022), article no. e42.

Get full text PDF Peer reviewed and recommended by PCI

In ambiguous stop/sense genetic codes, the stop codon(s) not only terminate translation but can also encode amino acids. Such codes have evolved at least four times in eukaryotes, twice among ciliates (Condylostoma magnum and Parduczia sp.). These have appeared to be isolated cases whose next closest relatives use conventional stop codons. However, little genomic data have been published for the Karyorelictea, the ciliate class that contains Parduczia sp., and previous studies may have overlooked ambiguous codes because of their apparent rarity. We therefore analyzed single-cell transcriptomes from four of the six karyorelict families to determine their genetic codes. Reassignment of canonical stops to sense codons was inferred from codon frequencies in conserved protein domains, while the actual stop codon was predicted from full-length transcripts with intact 3’-untranslated regions (3’-UTRs). We found that all available karyorelicts use the Parduczia code, where canonical stops UAA and UAG are reassigned to glutamine, and UGA encodes either tryptophan or stop. Furthermore, a small minority of transcripts may use an ambiguous stop-UAA instead of stop-UGA. Given the ubiquity of karyorelicts in marine coastal sediments, ambiguous genetic codes are not mere marginal curiosities but a defining feature of a globally distributed and diverse group of eukaryotes.

Published online:
DOI: 10.24072/pcjournal.141
Type: Research article
Seah, Brandon Kwee Boon 1; Singh, Aditi 1; Swart, Estienne Carl 1

1 Max Planck Institute for Biology, 72076 Tübingen, Germany
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
     author = {Seah, Brandon Kwee Boon and Singh, Aditi and Swart, Estienne Carl},
     title = {Karyorelict ciliates use an ambiguous genetic code with context-dependent stop/sense codons},
     journal = {Peer Community Journal},
     eid = {e42},
     publisher = {Peer Community In},
     volume = {2},
     year = {2022},
     doi = {10.24072/pcjournal.141},
     url = {}
AU  - Seah, Brandon Kwee Boon
AU  - Singh, Aditi
AU  - Swart, Estienne Carl
TI  - Karyorelict ciliates use an ambiguous genetic code with context-dependent stop/sense codons
JO  - Peer Community Journal
PY  - 2022
VL  - 2
PB  - Peer Community In
UR  -
DO  - 10.24072/pcjournal.141
ID  - 10_24072_pcjournal_141
ER  - 
%0 Journal Article
%A Seah, Brandon Kwee Boon
%A Singh, Aditi
%A Swart, Estienne Carl
%T Karyorelict ciliates use an ambiguous genetic code with context-dependent stop/sense codons
%J Peer Community Journal
%D 2022
%V 2
%I Peer Community In
%R 10.24072/pcjournal.141
%F 10_24072_pcjournal_141
Seah, Brandon Kwee Boon; Singh, Aditi; Swart, Estienne Carl. Karyorelict ciliates use an ambiguous genetic code with context-dependent stop/sense codons. Peer Community Journal, Volume 2 (2022), article  no. e42. doi : 10.24072/pcjournal.141.

PCI peer reviews and recommendation, and links to data, scripts, code and supplementary information: 10.24072/pci.genomics.100019

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Ivanova, N. N.; Schwientek, P.; Tripp, H. J.; Rinke, C.; Pati, A.; Huntemann, M.; Visel, A.; Woyke, T.; Kyrpides, N. C.; Rubin, E. M. Stop codon reassignments in the wild, Science, Volume 344 (2014) no. 6186, pp. 909-913 | DOI

[2] Shulgina, Y.; Eddy, S. R. A computational screen for alternative genetic codes in over 250,000 genomes, eLife, Volume 10 (2021) | DOI

[3] Kollmar, M.; Mühlhausen, S. Nuclear codon reassignments in the genomics era and mechanisms behind their evolution, BioEssays, Volume 39 (2017) no. 5 | DOI

[4] Schueren, F.; Thoms, S. Functional Translational Readthrough: A Systems Biology Perspective, PLOS Genetics, Volume 12 (2016) no. 8 | DOI

[5] Suzuki, T. The `polysemous' codon_a codon with multiple amino acid assignment caused by dual specificity of tRNA identity, The EMBO Journal, Volume 16 (1997) no. 5, pp. 1122-1134 | DOI

[6] Hatfield, D. L.; Gladyshev, V. N. How Selenium Has Altered Our Understanding of the Genetic Code, Molecular and Cellular Biology, Volume 22 (2002) no. 11, pp. 3565-3576 | DOI

[7] Záhonová, K.; Kostygov, A. Y.; Ševčíková, T.; Yurchenko, V.; Eliáš, M. An Unprecedented Non-canonical Nuclear Genetic Code with All Three Termination Codons Reassigned as Sense Codons, Current Biology, Volume 26 (2016) no. 17, pp. 2364-2369 | DOI

[8] Bachvaroff, T. R. A precedented nuclear genetic code with all three termination codons reassigned as sense codons in the syndinean Amoebophrya sp. ex Karlodinium veneficum, PLOS ONE, Volume 14 (2019) no. 2 | DOI

[9] Heaphy, S. M.; Mariotti, M.; Gladyshev, V. N.; Atkins, J. F.; Baranov, P. V. Novel Ciliate Genetic Code Variants Including the Reassignment of All Three Stop Codons to Sense Codons in<i>Condylostoma magnum</i>, Molecular Biology and Evolution, Volume 33 (2016) no. 11, pp. 2885-2889 | DOI

[10] Swart, E. C.; Serra, V.; Petroni, G.; Nowacki, M. Genetic Codes with No Dedicated Stop Codon: Context-Dependent Translation Termination, Cell, Volume 166 (2016) no. 3, pp. 691-702 | DOI

[11] Lozupone, C. A.; Knight, R. D.; Landweber, L. F. The molecular basis of nuclear genetic code change in ciliates, Current Biology, Volume 11 (2001) no. 2, pp. 65-74 | DOI

[12] Preer, J. R.; Preer, L. B.; Rudman, B. M.; Barnett, A. J. Deviation from the universal code shown by the gene for surface protein 51A in Paramecium, Nature, Volume 314 (1985) no. 6007, pp. 188-190 | DOI

[13] Horowitz, S.; Gorovsky, M. A. An unusual genetic code in nuclear genes of Tetrahymena., Proceedings of the National Academy of Sciences, Volume 82 (1985) no. 8, pp. 2452-2455 | DOI

[14] Meyer, F.; Schmidt, H. J.; Plümper, E.; Hasilik, A.; Mersmann, G.; Meyer, H. E.; Engström, A.; Heckmann, K. UGA is translated as cysteine in pheromone 3 of Euplotes octocarinatus., Proceedings of the National Academy of Sciences, Volume 88 (1991) no. 9, pp. 3758-3761 | DOI

[15] Tourancheau, A.; Tsao, N.; Klobutcher, L.; Pearlman, R.; Adoutte, A. Genetic code deviations in the ciliates: evidence for multiple and independent events., The EMBO Journal, Volume 14 (1995) no. 13, pp. 3262-3267 | DOI

[16] Helftenbem, E. Nucleotide sequence of a macronuclear DNA molecule coding for α-tubulin from the ciliate<i>Stylonychia lemnae</i>. Special codon usage: TAA is not a translation termination codon, Nucleic Acids Research, Volume 13 (1985) no. 2, pp. 415-433 | DOI

[17] Yan, Y.; Maurer-Alcalá, X. X.; Knight, R.; Kosakovsky Pond, S. L.; Katz, L. A. Single-Cell Transcriptomics Reveal a Correlation between Genome Architecture and Gene Family Evolution in Ciliates, mBio, Volume 10 (2019) no. 6 | DOI

[18] Raikov, I. B. Primitive Never-Dividing Macronuclei of Some Lower Ciliates, International Review of Cytology, Volume 95, Elsevier, 1985, pp. 267-325 | DOI

[19] Fenchel, T. The ecology of marine microbenthos IV. Structure and function of the benthic ecosystem, its chemical and physical factors and the microfauna commuities with special reference to the ciliated protozoa, Ophelia, Volume 6 (1969) no. 1, pp. 1-182 | DOI

[20] Ma, M.; Li, Y.; Maurer-Alcalá, X. X.; Wang, Y.; Yan, Y. Deciphering phylogenetic relationships in class Karyorelictea (Protista, Ciliophora) based on updated multi-gene information with establishment of a new order Wilbertomorphida n. ord., Molecular Phylogenetics and Evolution, Volume 169 (2022) | DOI

[21] Foissner, W. The karyorelictids (Protozoa: Ciliophora), a unique and enigmatic assemblage of marine, interstitial ciliates: a review emphasizing ciliary patterns and evolution. Evolutionary relationships among Protozoa In: Evolutionary Relationships Among Protozoa., Chapman & Hall, London, UK (1998), pp. 305-325

[22] Seah, B. K. B.; Singh, A.; Swart, E. C. Edmond, 2022 | DOI

[23] Waterhouse, R. M.; Seppey, M.; Simão, F. A.; Manni, M.; Ioannidis, P.; Klioutchnikov, G.; Kriventseva, E. V.; Zdobnov, E. M. BUSCO Applications from Quality Assessments to Gene Prediction and Phylogenomics, Molecular Biology and Evolution, Volume 35 (2018) no. 3, pp. 543-548 | DOI

[24] Xu, Y.; Li, J.; Song, W.; Warren, A. Phylogeny and Establishment of a New Ciliate Family, Wilbertomorphidae fam. nov. (Ciliophora, Karyorelictea), a Highly Specialized Taxon Represented by <i>Wilbertomorpha colpoda</i> gen. nov., spec. nov., Journal of Eukaryotic Microbiology, Volume 60 (2013) no. 5, pp. 480-489 | DOI

[25] Fernandes, N. M.; Schrago, C. G. A multigene timescale and diversification dynamics of Ciliophora evolution, Molecular Phylogenetics and Evolution, Volume 139 (2019) | DOI

[26] Singh, M.; Brandon Seah, K. B.; Emmerich, C.; Singh, A.; Woehle, C.; Huettel, B.; Byerly, A.; Stover, N. A.; Sugiura, M.; Harumoto, T.; Swart, E. C. Genome editing excisase origins illuminated by somatic genome of <i>Blepharisma</i>, bioRxiv, 2021 | DOI

[27] Alkalaeva, E.; Mikhailova, T. Reassigning stop codons via translation termination: How a few eukaryotes broke the dogma, BioEssays, Volume 39 (2017) no. 3 | DOI

[28] Eliseev, B. D.; Alkalaeva, E. Z.; Kryuchkova, P. N.; Lekomtsev, S. A.; Wang, W.; Liang, A.-H.; Frolova, L. Y. Translation termination factor eRF1 of the ciliate Blepharisma japonicum recognizes all three stop codons, Molecular Biology, Volume 45 (2011) no. 4, pp. 614-618 | DOI

[29] Fleming, I.; Cavalcanti, A. R. O. Selection for tandem stop codons in ciliate species with reassigned stop codons, PLOS ONE, Volume 14 (2019) no. 11 | DOI

[30] Crick, F. The origin of the genetic code, Journal of Molecular Biology, Volume 38 (1968) no. 3, pp. 367-379 | DOI

[31] Seah, B. K. B.; Antony, C. P.; Huettel, B.; Zarzycki, J.; Schada von Borzyskowski, L.; Erb, T. J.; Kouris, A.; Kleiner, M.; Liebeke, M.; Dubilier, N.; Gruber-Vodicka, H. R. Sulfur-Oxidizing Symbionts without Canonical Genes for Autotrophic CO <sub>2</sub> Fixation, mBio, Volume 10 (2019) no. 3 | DOI

[32] Keeling, P. J.; Burki, F.; Wilcox, H. M.; Allam, B.; Allen, E. E.; Amaral-Zettler, L. A.; Armbrust, E. V.; Archibald, J. M.; Bharti, A. K.; Bell, C. J.; Beszteri, B.; Bidle, K. D.; Cameron, C. T.; Campbell, L.; Caron, D. A.; Cattolico, R. A.; Collier, J. L.; Coyne, K.; Davy, S. K.; Deschamps, P.; Dyhrman, S. T.; Edvardsen, B.; Gates, R. D.; Gobler, C. J.; Greenwood, S. J.; Guida, S. M.; Jacobi, J. L.; Jakobsen, K. S.; James, E. R.; Jenkins, B.; John, U.; Johnson, M. D.; Juhl, A. R.; Kamp, A.; Katz, L. A.; Kiene, R.; Kudryavtsev, A.; Leander, B. S.; Lin, S.; Lovejoy, C.; Lynn, D.; Marchetti, A.; McManus, G.; Nedelcu, A. M.; Menden-Deuer, S.; Miceli, C.; Mock, T.; Montresor, M.; Moran, M. A.; Murray, S.; Nadathur, G.; Nagai, S.; Ngam, P. B.; Palenik, B.; Pawlowski, J.; Petroni, G.; Piganeau, G.; Posewitz, M. C.; Rengefors, K.; Romano, G.; Rumpho, M. E.; Rynearson, T.; Schilling, K. B.; Schroeder, D. C.; Simpson, A. G. B.; Slamovits, C. H.; Smith, D. R.; Smith, G. J.; Smith, S. R.; Sosik, H. M.; Stief, P.; Theriot, E.; Twary, S. N.; Umale, P. E.; Vaulot, D.; Wawrik, B.; Wheeler, G. L.; Wilson, W. H.; Xu, Y.; Zingone, A.; Worden, A. Z. The Marine Microbial Eukaryote Transcriptome Sequencing Project (MMETSP): Illuminating the Functional Diversity of Eukaryotic Life in the Oceans through Transcriptome Sequencing, PLoS Biology, Volume 12 (2014) no. 6 | DOI

[33] Kolisko, M.; Boscaro, V.; Burki, F.; Lynn, D. H.; Keeling, P. J. Single-cell transcriptomics for microbial eukaryotes, Current Biology, Volume 24 (2014) no. 22 | DOI

[34] Quast, C.; Pruesse, E.; Yilmaz, P.; Gerken, J.; Schweer, T.; Yarza, P.; Peplies, J.; Glöckner, F. O. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools, Nucleic Acids Research, Volume 41 (2013) | DOI

[35] Gruber-Vodicka, H. R.; Seah, B. K. B.; Pruesse, E. phyloFlash: Rapid Small-Subunit rRNA Profiling and Targeted Assembly from Metagenomes, mSystems, Volume 5 (2020) no. 5 | DOI

[36] Grabherr, M. G.; Haas, B. J.; Yassour, M.; Levin, J. Z.; Thompson, D. A.; Amit, I.; Adiconis, X.; Fan, L.; Raychowdhury, R.; Zeng, Q.; Chen, Z.; Mauceli, E.; Hacohen, N.; Gnirke, A.; Rhind, N.; di Palma, F.; Birren, B. W.; Nusbaum, C.; Lindblad-Toh, K.; Friedman, N.; Regev, A. Full-length transcriptome assembly from RNA-Seq data without a reference genome, Nature Biotechnology, Volume 29 (2011) no. 7, pp. 644-652 | DOI

[37] Camacho, C.; Coulouris, G.; Avagyan, V.; Ma, N.; Papadopoulos, J.; Bealer, K.; Madden, T. L. BLAST+: architecture and applications, BMC Bioinformatics, Volume 10 (2009) no. 1 | DOI

[38] Tange, O. Zenodo | DOI

[39] Guillou, L.; Bachar, D.; Audic, S.; Bass, D.; Berney, C.; Bittner, L.; Boutte, C.; Burgaud, G.; de Vargas, C.; Decelle, J.; del Campo, J.; Dolan, J. R.; Dunthorn, M.; Edvardsen, B.; Holzmann, M.; Kooistra, W. H.; Lara, E.; Le Bescot, N.; Logares, R.; Mahé, F.; Massana, R.; Montresor, M.; Morard, R.; Not, F.; Pawlowski, J.; Probert, I.; Sauvadet, A.-L.; Siano, R.; Stoeck, T.; Vaulot, D.; Zimmermann, P.; Christen, R. The Protist Ribosomal Reference database (PR2): a catalog of unicellular eukaryote Small Sub-Unit rRNA sequences with curated taxonomy, Nucleic Acids Research, Volume 41 (2013) no. D1 | DOI

[40] Rognes, T.; Flouri, T.; Nichols, B.; Quince, C.; Mahé, F. VSEARCH: a versatile open source tool for metagenomics, PeerJ, Volume 4 (2016) | DOI

[41] Katoh, K.; Standley, D. M. MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability, Molecular Biology and Evolution, Volume 30 (2013) no. 4, pp. 772-780 | DOI

[42] Minh, B. Q.; Schmidt, H. A.; Chernomor, O.; Schrempf, D.; Woodhams, M. D.; von Haeseler, A.; Lanfear, R. IQ-TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era, Molecular Biology and Evolution, Volume 37 (2020) no. 5, pp. 1530-1534 | DOI

[43] Kalyaanamoorthy, S.; Minh, B. Q.; Wong, T. K. F.; von Haeseler, A.; Jermiin, L. S. ModelFinder: fast model selection for accurate phylogenetic estimates, Nature Methods, Volume 14 (2017) no. 6, pp. 587-589 | DOI

[44] Seah, B. K. B.; Singh, A.; Swart, E. C. Edmond, 2022 | DOI

[45] Mölder, F.; Jablonski, K. P.; Letcher, B.; Hall, M. B.; Tomkins-Tinch, C. H.; Sochat, V.; Forster, J.; Lee, S.; Twardziok, S. O.; Kanitz, A.; Wilm, A.; Holtgrewe, M.; Rahmann, S.; Nahnsen, S.; Köster, J. Sustainable data analysis with Snakemake, F1000Research, Volume 10 (2021) | DOI

[46] Seah, B. K. B. Zenodo, 2022 | DOI

[47] Cock, P. J. A.; Antao, T.; Chang, J. T.; Chapman, B. A.; Cox, C. J.; Dalke, A.; Friedberg, I.; Hamelryck, T.; Kauff, F.; Wilczynski, B.; de Hoon, M. J. L. Biopython: freely available Python tools for computational molecular biology and bioinformatics, Bioinformatics, Volume 25 (2009) no. 11, pp. 1422-1423 | DOI

[48] McKinney, W. Data Structures for Statistical Computing in Python, SciPy, Proceedings of the Python in Science Conference (2010) | DOI

[49] Waskom, M. seaborn: statistical data visualization, Journal of Open Source Software, Volume 6 (2021) no. 60 | DOI

[50] Hunter, J. D. Matplotlib: A 2D Graphics Environment, Computing in Science &amp; Engineering, Volume 9 (2007) no. 3, pp. 90-95 | DOI

[51] Swart, E. C.; Seah, B. K. B. Zenodo, 2022 | DOI

[52] Seah, B. K. B. Zenodo, 2022 | DOI

[53] Dutilh, B. E.; Jurgelenaite, R.; Szklarczyk, R.; van Hijum, S. A.; Harhangi, H. R.; Schmid, M.; de Wild, B.; Françoijs, K.; Stunnenberg, H. G.; Strous, M.; Jetten, M. S.; Op den Camp, H. J.; Huynen, M. A. FACIL: Fast and Accurate Genetic Code Inference and Logo, Bioinformatics, Volume 27 (2011) no. 14, pp. 1929-1933 | DOI

[54] Mistry, J.; Chuguransky, S.; Williams, L.; Qureshi, M.; Salazar, G. A.; Sonnhammer, E. L. L.; Tosatto, S. C. E.; Paladin, L.; Raj, S.; Richardson, L. J.; Finn, R. D.; Bateman, A. Pfam: The protein families database in 2021, Nucleic Acids Research, Volume 49 (2021) no. D1 | DOI

[55] Crooks, G. E.; Hon, G.; Chandonia, J.-M.; Brenner, S. E. WebLogo: A Sequence Logo Generator: Figure 1, Genome Research, Volume 14 (2004) no. 6, pp. 1188-1190 | DOI

[56] Aury, J.-M.; Jaillon, O.; Duret, L.; Noel, B.; Jubin, C.; Porcel, B. M.; Ségurens, B.; Daubin, V.; Anthouard, V.; Aiach, N.; Arnaiz, O.; Billaut, A.; Beisson, J.; Blanc, I.; Bouhouche, K.; Câmara, F.; Duharcourt, S.; Guigo, R.; Gogendeau, D.; Katinka, M.; Keller, A.-M.; Kissmehl, R.; Klotz, C.; Koll, F.; Le Mouël, A.; Lepère, G.; Malinsky, S.; Nowacki, M.; Nowak, J. K.; Plattner, H.; Poulain, J.; Ruiz, F.; Serrano, V.; Zagulski, M.; Dessen, P.; Bétermier, M.; Weissenbach, J.; Scarpelli, C.; Schächter, V.; Sperling, L.; Meyer, E.; Cohen, J.; Wincker, P. Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia, Nature, Volume 444 (2006) no. 7116, pp. 171-178 | DOI

[57] Slabodnick, M. M.; Ruby, J. G.; Reiff, S. B.; Swart, E. C.; Gosai, S.; Prabakaran, S.; Witkowska, E.; Larue, G. E.; Fisher, S.; Freeman, R. M.; Gunawardena, J.; Chu, W.; Stover, N. A.; Gregory, B. D.; Nowacki, M.; Derisi, J.; Roy, S. W.; Marshall, W. F.; Sood, P. The Macronuclear Genome of Stentor coeruleus Reveals Tiny Introns in a Giant Cell, Current Biology, Volume 27 (2017) no. 4, pp. 569-575 | DOI

[58] Arnaiz, O.; Meyer, E.; Sperling, L. ParameciumDB 2019: integrating genomic data across the genus for functional and evolutionary biology, Nucleic Acids Research, Volume 48 (2020) | DOI

[59] Sheng, Y.; Duan, L.; Cheng, T.; Qiao, Y.; Stover, N. A.; Gao, S. The completed macronuclear genome of a model ciliate Tetrahymena thermophila and its application in genome scrambling and copy number analyses, Science China Life Sciences, Volume 63 (2020) no. 10, pp. 1534-1542 | DOI

[60] Stover, N. A. Tetrahymena Genome Database (TGD): a new genomic resource for Tetrahymena thermophila research, Nucleic Acids Research, Volume 34 (2006) no. 90001 | DOI

[61] Seah, B. K. B. Zenodo, 2022 | DOI

[62] Chen, X.; Jiang, Y.; Gao, F.; Zheng, W.; Krock, T. J.; Stover, N. A.; Lu, C.; Katz, L. A.; Song, W. Genome analyses of the new model protist <i>Euplotes vannus</i> focusing on genome rearrangement and resistance to environmental stressors, Molecular Ecology Resources, Volume 19 (2020) no. 5, pp. 1292-1308 | DOI

[63] Coyne, R. S.; Hannick, L.; Shanmugam, D.; Hostetler, J. B.; Brami, D.; Joardar, V. S.; Johnson, J.; Radune, D.; Singh, I.; Badger, J. H.; Kumar, U.; Saier, M.; Wang, Y.; Cai, H.; Gu, J.; Mather, M. W.; Vaidya, A. B.; Wilkes, D. E.; Rajagopalan, V.; Asai, D. J.; Pearson, C. G.; Findly, R. C.; Dickerson, H. W.; Wu, M.; Martens, C.; Van de Peer, Y.; Roos, D. S.; Cassidy-Hanley, D. M.; Clark, T. G. 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 Biology, Volume 12 (2011) no. 10 | DOI

[64] Swart, E. C.; Bracht, J. R.; Magrini, V.; Minx, P.; Chen, X.; Zhou, Y.; Khurana, J. S.; Goldman, A. D.; Nowacki, M.; Schotanus, K.; Jung, S.; Fulton, R. S.; Ly, A.; McGrath, S.; Haub, K.; Wiggins, J. L.; Storton, D.; Matese, J. C.; Parsons, L.; Chang, W.-J.; Bowen, M. S.; Stover, N. A.; Jones, T. A.; Eddy, S. R.; Herrick, G. A.; Doak, T. G.; Wilson, R. K.; Mardis, E. R.; Landweber, L. F. The Oxytricha trifallax Macronuclear Genome: A Complex Eukaryotic Genome with 16,000 Tiny Chromosomes, PLoS Biology, Volume 11 (2013) no. 1 | DOI

[65] Xiong, J.; Wang, G.; Cheng, J.; Tian, M.; Pan, X.; Warren, A.; Jiang, C.; Yuan, D.; Miao, W. Genome of the facultative scuticociliatosis pathogen Pseudocohnilembus persalinus provides insight into its virulence through horizontal gene transfer, Scientific Reports, Volume 5 (2015) no. 1 | DOI

[66] Aeschlimann, S. H.; Jönsson, F.; Postberg, J.; Stover, N. A.; Petera, R. L.; Lipps, H.-J.; Nowacki, M.; Swart, E. C. The Draft Assembly of the Radically Organized Stylonychia lemnae Macronuclear Genome, Genome Biology and Evolution, Volume 6 (2014) no. 7, pp. 1707-1723 | DOI

[67] Hamilton, E. P.; Kapusta, A.; Huvos, P. E.; Bidwell, S. L.; Zafar, N.; Tang, H.; Hadjithomas, M.; Krishnakumar, V.; Badger, J. H.; Caler, E. V.; Russ, C.; Zeng, Q.; Fan, L.; Levin, J. Z.; Shea, T.; Young, S. K.; Hegarty, R.; Daza, R.; Gujja, S.; Wortman, J. R.; Birren, B. W.; Nusbaum, C.; Thomas, J.; Carey, C. M.; Pritham, E. J.; Feschotte, C.; Noto, T.; Mochizuki, K.; Papazyan, R.; Taverna, S. D.; Dear, P. H.; Cassidy-Hanley, D. M.; Xiong, J.; Miao, W.; Orias, E.; Coyne, R. S. Structure of the germline genome of Tetrahymena thermophila and relationship to the massively rearranged somatic genome, eLife, Volume 5 (2016) | DOI

[68] McGrath, C. L.; Gout, J.-F.; Doak, T. G.; Yanagi, A.; Lynch, M. Insights into Three Whole-Genome Duplications Gleaned from the <i>Paramecium caudatum</i> Genome Sequence, Genetics, Volume 197 (2014) no. 4, pp. 1417-1428 | DOI

[69] Arnaiz, O.; Van Dijk, E.; Bétermier, M.; Lhuillier-Akakpo, M.; de Vanssay, A.; Duharcourt, S.; Sallet, E.; Gouzy, J.; Sperling, L. Improved methods and resources for paramecium genomics: transcription units, gene annotation and gene expression, BMC Genomics, Volume 18 (2017) no. 1 | DOI

[70] Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput, Nucleic Acids Research, Volume 32 (2004) no. 5, pp. 1792-1797 | DOI

[71] Yan, Y.; Xu, Y.; Al-Farraj, S. A.; Al-Rasheid, K. A. S.; Song, W. Morphology and phylogeny of three trachelocercids (Protozoa, Ciliophora, Karyorelictea), with description of two new species and insight into the evolution of the family Trachelocercidae, Zoological Journal of the Linnean Society, Volume 177 (2016) no. 2, pp. 306-319 | DOI

[72] Xu, Y.; Gao, S.; Hu, X.; Al-Rasheid, K. A.; Song, W. Phylogeny and systematic revision of the karyorelictid genus Remanella (Ciliophora, Karyorelictea) with descriptions of two new species, European Journal of Protistology, Volume 49 (2013) no. 3, pp. 438-452 | DOI

Cited by Sources: