Phylogenomic analyses reveal subclass Scuticociliatia as the sister group of subclass Hymenostomatia within class Oligohymenophorea

Molecular Phylogenetics and Evolution

Volumn 90, Issue , 2015, Pages 104-111

  Feng, Jin Mei ^a,b   Jiang, Chuan Qi ^b   Warren, Alan ^c   Tian, Miao ^b   Cheng, Jun ^b,d   Liu, Guang Long ^b   Xiong, Jie ^b   Miao, Wei ^b  

^a JIANGHAN UNIVERSITY   (China)

^b INSTITUTE OF HYDROBIOLOGY   (China)

^c DEPARTMENT OF LIFE SCIENCES   (United Kingdom)

^d GUANGDONG OCEAN UNIVERSITY   (China)

Author keywords

Hymenostomatia; Oligohymenophorea; Phylogenomics analysis; Scuticociliatia

Indexed keywords

CILIOPHORA; COLPODEA; HYMENOSTOMATIA; HYMENOSTOMATIDA; OLIGOHYMENOPHOREA; PARAMECIUM; SCUTICOCILIATIA; TETRAHYMENA; TETRAHYMENA THERMOPHILA;

RNA; TRANSCRIPTOME;

CILIATE; CLASSIFICATION; GENETICS; ISOLATION AND PURIFICATION; NUCLEOTIDE SEQUENCE; OLIGOHYMENOPHOREA; PHYLOGENY; SEQUENCE ANALYSIS;

BASE SEQUENCE; CILIOPHORA; OLIGOHYMENOPHOREA; PHYLOGENY; RNA; SEQUENCE ANALYSIS, RNA; TRANSCRIPTOME;

EID: 84930210577     PISSN: 10557903     EISSN: 10959513     Source Type: Journal    
DOI: 10.1016/j.ympev.2015.05.007     Document Type: Article

References (74)

1. Abdel-Hafez G., Lahnsteiner F., Mansour N., Licek E. Pathophysiology of Ichthyophthirius multifiliis Infection in Rainbow Trout (Oncorhynchus mykiss) and Chub (Leuciscus cephalus). J. Comp. Pathol. 2014, 151:394-399.
2. Abernathy J.W., Xu P., Li P., Xu D.H., Kucuktas H., Klesius P., Arias C., Liu Z. Generation and analysis of expressed sequence tags from the ciliate protozoan parasite Ichthyophthirius multifiliis. BMC Genom. 2007, 8:176.
3. Aeschlimann S.H., Jonsson 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 Biol. Evol. 2014, 6:1707-1723.
4. Al-Rasheid K.A.S. Redescription of the marine ciliate Cardiostomatella vermiforme (Kahl, 1928) Corliss, 1960. Protistology 2001, 2:15-21.
5. Asai D.J., Forney J.D. Tetrahymena Thermophila 2000, Academic Press, San Diego, 580p.
6. Aury J.M., Jaillon O., Duret L., Noel B., Jubin C., Porcel B.M., Segurens B., Daubin V., Anthouard V., Aiach N., Arnaiz O., Billaut A., Beisson J., Blanc I., Bouhouche K., Camara F., Duharcourt S., Guigo R., Gogendeau D., Katinka M., Keller A.M., Kissmehl R., Klotz C., Koll F., Le Mouel A., Lepere G., Malinsky S., Nowacki M., Nowak J.K., Plattner H., Poulain J., Ruiz F., Serrano V., Zagulski M., Dessen P., Betermier M., Weissenbach J., Scarpelli C., Schachter V., Sperling L., Meyer E., Cohen J., Wincker P. Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia. Nature 2006, 444:171-178.
7. Bardele C.F. Functional and phylogenetic aspects of the ciliary membrane: a comparative freeze-fracture study. Biosystems 1981, 14:403-421.
8. Brown M.W., Sharpe S.C., Silberman J.D., Heiss A.A., Lang B.F., Simpson A.G., Roger A.J. Phylogenomics demonstrates that breviate flagellates are related to opisthokonts and apusomonads. Proc. Biol. Sci. 2013, 280:20131755.
9. Burki F., Shalchian-Tabrizi K., Minge M., Skjaeveland A., Nikolaev S.I., Jakobsen K.S., Pawlowski J. Phylogenomics reshuffles the eukaryotic supergroups. PLoS ONE 2007, 2.
10. Burki F., Inagaki Y., Brate J., Archibald J.M., Keeling P.J., Cavalier-Smith T., Sakaguchi M., Hashimoto T., Horak A., Kumar S., Klaveness D., Jakobsen K.S., Pawlowski J., Shalchian-Tabrizi K. Large-scale phylogenomic analyses reveal that two enigmatic protist lineages, Telonemia and Centroheliozoa, are related to photosynthetic Chromalveolates. Genome Biol. Evol. 2009, 1:231-238.
11. Burki F., Okamoto N., Pombert J.F., Keeling P.J. The evolutionary history of haptophytes and cryptophytes: phylogenomic evidence for separate origins. Proc. Roy. Soc. B 2012, 279:2246-2254.
12. Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 2000, 17:540-552.
13. Chiari Y., Cahais V., Galtier N., Delsuc F. Phylogenomic analyses support the position of turtles as the sister group of birds and crocodiles (Archosauria). BMC Biol. 2012, 10.
14. Corliss J.O. History, taxonomy, ecology, and evolution of species of Tetrahymena. Biology of Tetrahymena, Dowden 1973, 1-55. Hutchinson & Ross, Stroudsburg, PA. A.M. Elliott (Ed.).
15. Corliss J.O. The Ciliated Protozoa: Characterization, Classification, and Guide to the Literature 1979, Pergamon Press, London/New York, 455pp. second ed.
16. Dias R.J.P., Cabral A.F., Siqueira-Castro I.C.V., Silva-Neto I.D.d., D'Agosto M. Morphometric study of a Brazilian strain of Carchesium polypinum (Ciliophora: Peritrichia) attached to Pomacea figulina (Mollusca: Gastropoda), with notes on a high infestation. Zoologia (Curitiba, Impresso) 2010, 27:483-488.
17. Edgar R.C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004, 32:1792-1797.
18. Evans N.M., Holder M.T., Barbeitos M.S., Okamura B., Cartwright P. The phylogenetic position of Myxozoa: exploring conflicting signals in phylogenomic and ribosomal data sets. Mol. Biol. Evol. 2010, 27:2733-2746.
19. Feng J.M., Xiong J., Zhang J.Y., Yang Y.L., Yao B., Zhou Z.G., Miao W. New phylogenomic and comparative analyses provide corroborating evidence that Myxozoa is Cnidaria. Mol. Phylogenet. Evol. 2014, 81:10-18.
20. Foissner W., Berger H., Kohmann F. Taxonomische undökologische Revision der Ciliaten des Saprobiensystems - BandII: Peritrichia, Heterotrichida, Odontostomatida. Informations-berichte des Bayer. Landesamtes für Wasserwirtschaft 1992, 5:1-502.
21. Forwood J.M., Harris J.O., Landos M., Deveney M.R. Minimum effective concentrations of formalin and sodium percarbonate on the free-living stages of an Australian isolate of Ichthyophthirius multifiliis. Parasitol. Res. 2014, 113:3251-3258.
22. Fu Y., Zhang Q., Xu D.H., Xia H., Cai X., Wang B., Liang J. Parasiticidal effects of Morus alba root bark extracts against Ichthyophthirius multifiliis infecting grass carp. Dis. Aquat. Org. 2014, 108:129-136.
23. Gao F., Katz L.A., Song W. Multigene-based analyses on evolutionary phylogeny of two controversial ciliate orders: Pleuronematida and Loxocephalida (Protista, Ciliophora, Oligohymenophorea). Mol. Phylogenet. Evol. 2013, 68:55-63.
24. Gentekaki E., Kolisko M., Boscaro V., Bright K.J., Dini F., Di Giuseppe G., Gong Y., Miceli C., Modeo L., Molestina R.E., Petroni G., Pucciarelli S., Roger A.J., Strom S.L., Lynn D.H. Large-scale phylogenomic analysis reveals the phylogenetic position of the problematic taxon Protocruzia and unravels the deep phylogenetic affinities of the ciliate lineages. Mol. Phylogenet. Evol. 2014, 78C:36-42.
25. 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. Nat. Biotechnol. 2011, 29:644-652.
26. Hampl V., Hug L., Leigh J.W., Dacks J.B., Lang B.F., Simpson A.G., Roger A.J. Phylogenomic analyses support the monophyly of Excavata and resolve relationships among eukaryotic "supergroups". Proc. Natl. Acad. Sci. U.S.A. 2009, 106:3859-3864.
27. Harikrishnan R., Balasundaram C., Heo M.S. Scuticociliatosis and its recent prophylactic measures in aquaculture with special reference to South Korea Taxonomy, diversity and diagnosis of scuticociliatosis: Part I Control strategies of scuticociliatosis: Part II. Fish Shellfish Immunol. 2010, 29:15-31.
28. Hoshino M.D., Hoshino E.M., Tavares-Dias M. First study on parasites of Hemibrycon surinamensis (Characidae), a host from the eastern Amazon region. Rev. Bras. Parasitol. Vet. 2014, 23:343-347.
29. Jin C.N., Harikrishnan R., Moon Y.G., Kim M.C., Kim J.S., Balasundaram C., Heo M.S. Effectiveness of chemotherapeutants against scuticociliate Philasterides dicentrarchi, a parasite of olive flounder. Vet. Parasitol. 2010, 168:19-24.
30. Lartillot N., Lepage T., Blanquart S. PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating. Bioinformatics 2009, 25:2286-2288.
31. Li L., Song W., Warren A., Wang Y., Ma H., Hu X., Chen Z. Phylogenetic position of the marine ciliate, Cardiostomatella vermiforme (Kahl, 1928) Corliss, 1960 inferred from the complete SSrRNA gene sequence, with establishment of a new order Loxocephalida n. ord. (Ciliophora, Oligohymenophorea). Eur. J. Protistol. 2006, 42:107-114.
32. Li J., Lin X., Yi Z., Clamp J.C., Liu W., Al-Rasheid K.A.S. Molecules or morphogenesis: how to determine the phylogenetic assignment of Paratetrahymena (Protista, Ciliophora, Oligohymenophorea)?. Zoolog. Scr. 2010, 39:499-510.
33. Liang D., Shen X.X., Zhang P. One thousand two hundred ninety nuclear genes from a genome-wide survey support lungfishes as the sister group of tetrapods. Mol. Biol. Evol. 2013, 30:1803-1807.
34. Lynn D.H. Morphology or molecules: How do we identify the major lineages of ciliates (Phylum Ciliophora). Eur. J. Protistol. 2003, 39:356-364.
35. Lynn D. The ciliated protozoa: characterization, classification and guide to the literature 2008, Springer, Dordrecht, The Netherlands. third ed.
36. Lynn D.H., Small E.B. A revised classification of the phylum Ciliophora Doflein, 1901. Revista de la Sociedad Mexicana de Historia Natural 1997, 47.
37. Lynn, D.H., Small, E.B., 2002. Phylum Ciliophora, Doflein, 1901. In: Lee, J.J., Leedale, G.F., Bradbury, P.C. (Eds.), An illustrated guide to the protozoa (2000). Kansas, USA, Society of Protozoologists, Lawrence, vol. 1, pp. 371-656.
38. Lynn D.H., Sogin M.L. Assessment of phylogenetic relationships among ciliated protists using partial ribosomal RNA sequences derived from reverse transcripts. Biosystems 1988, 21:249-254.
39. Maddison, W.P., Maddison, D.R., 2011. Mesquite: a modular system for evolutionary analysis. Version 2.75 .
40. Miao W., Yu Y.H., Shen Y.F. Phylogenetic relationships of the subclass peritrichia (Oligohymenophorea, Ciliophora) with emphasis on the genus Epistylis, inferred from small subunit rRNA gene sequences. J. Eukaryot. Microbiol. 2001, 48:583-587.
41. Miao W., Fen W.S., Yu Y.H., Zhang X.Y., Shen Y.F. Phylogenetic relationships of the subclass Peritrichia (Oligohymenophorea, Ciliophora) inferred from small subunit rRNA gene sequences. J. Eukaryot. Microbiol. 2004, 51:180-186.
42. Munday B.L., O'Donoghue P.J., Watts M., Rough K., Hawkesford T. Fatal encephalitis due to the scuticociliate Uronema nigricans in sea-caged, southern bluefin tuna Thunnus maccoyii. Dis. Aquat. Org. 1997, 30:17-25.
43. Philippe H., Telford M.J. Large-scale sequencing and the new animal phylogeny. Trends Ecol. Evol. 2006, 21:614-620.
44. Philippe H., Sörhannus U., Baroin A., Perasso R., Gasse F., Adoutte A. Comparison of molecular and paleontological data in diatoms suggests a major gap in the fossil record. J Evol Biol 1994, 7:247-265.
45. Philippe H., Lartillot N., Brinkmann H. Multigene analyses of bilaterian animals corroborate the monophyly of Ecdysozoa, Lophotrochozoa, and Protostomia. Mol. Biol. Evol. 2005, 22:1246-1253.
46. Philippe H., Derelle R., Lopez P., Pick K., Borchiellini C., Boury-Esnault N., Vacelet J., Renard E., Houliston E., Queinnec E., Da Silva C., Wincker P., Le Guyader H., Leys S., Jackson D.J., Schreiber F., Erpenbeck D., Morgenstern B., Worheide G., Manuel M. Phylogenomics revives traditional views on deep animal relationships. Curr. Biol. 2009, 19:706-712.
47. Posada D. JModelTest: phylogenetic model averaging. Mol. Biol. Evol. 2008, 25:1253-1256.
48. Ricard G., de Graaf R.M., Dutilh B.E., Duarte I., van Alen T.A., van Hoek A.H., Boxma B., van der Staay G.W., Moon-van der Staay S.Y., Chang W.J., Landweber L.F., Hackstein J.H., Huynen M.A. Macronuclear genome structure of the ciliate Nyctotherus ovalis: single-gene chromosomes and tiny introns. BMC Genom. 2008, 9:587.
49. Rice P., Bleasby A., Ison J., Mullan L., Bottu G. EMBOSS User's Guide: Practical Bioinformatics 2011, Cambridge Univ Press.
50. Ronquist F., Huelsenbeck J.P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-1574.
51. Roure B., Rodriguez-Ezpeleta N., Philippe H. SCaFoS: a tool for selection, concatenation and fusion of sequences for phylogenomics. BMC Evol. Biol. 2007, 7(Suppl 1):S2.
52. Ryan, J.F., Pang, K., Schnitzler, C.E., Nguyen, A.D., Moreland, R.T., Simmons, D.K., Koch, B.J., Francis, W.R., Havlak, P., Smith, S.A., Putnam, N.H., Haddock, S.H.D., Dunn, C.W., Wolfsberg, T.G., Mullikin, J.C., Martindale, M.Q., Baxevanis, A.D., Progra, N.C.S., 2013. The Genome of the Ctenophore Mnemiopsis leidyi and Its Implications for Cell Type Evolution. Science 342, 1336.
53. Sanchez-Silva R., Villalobo E., Morin L., Torres A. A new noncanonical nuclear genetic code: translation of UAA into glutamate. Curr. Biol. 2003, 13:442-447.
54. Shi X., Frankel J. Morphology and development of mirror image doubles ofStylonychia mytilus. J. Protozool. 1990, 37:1-13.
55. Shi X., Warren A., Yu Y., Shen Y. Infraciliature and myoneme system of Campanella umbellaria (Protozoa, Ciliophora, Peritrichida). J. Morphol. 2004, 261:43-51.
56. Shi T., Shi X., Lu F., Yu F., Fu Y., Hu X. A Colpoda aspera isolate from animal faeces: In vitro cultivation and identification. Eur. J. Protistol. 2014, 50:33-39.
57. Shimodaira H., Hasegawa M. CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 2001, 17:1246-1247.
58. Small E.B., Lynn D.H. A new macrosystem for the phylum Ciliophora doflein, 1901. Biosystems 1981, 14:387-401.
59. Small E.B., Lynn D.H. Phylum ciliophora, doflein, 1901. An Illustrated Guide to the Protozoa 1985, 393-575. Society of Protozoologists, Lawrence, Kansas, USA. J.J. Lee, S.H. Hutner, E.C. Bovee (Eds.).
60. Small E.B., Heisler J., Sniezek J., Iliffe T.M. Glauconema bermudense n. Sp. (Scuticociliatida, Oligohymenophorea), a troglobitic ciliophoran from Bermudian marine caves. Stygologia 1986, 167-179.
61. Song W.B., Zhao Y.J., Xu K.D., Hu X.Z., Gong J. Pathogenic Protozoa in Mariculture 2003, Science Press, Beijing.
62. Song W., Warren A., Roberts D., Ma H., Shang H., Wilbert N., Miao M., Yi Z. Re-evaluation of the phylogenetic position of the genus Dexiotrichides (Protozoa, Ciliophora, Scuticociliatida) inferred from stomatogenetic and molecular information for Dexiotrichides pangi. Prog. Nat. Sci. 2005, 15:700-707.
63. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006, 22:2688-2690.
64. Struck T.H., Fisse F. Phylogenetic position of Nemertea derived from phylogenomic data. Mol. Biol. Evol. 2008, 25:728-736.
65. Struder-Kypke M.C., Wright A.D., Fokin S.I., Lynn D.H. Phylogenetic relationships of the Subclass Peniculia (Oligohymenophorea, Ciliophora) inferred from small subunit rRNA gene sequences. J. Eukaryot. Microbiol. 2000, 47:419-429.
66. 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 Biol. 2013, 11:e1001473.
67. Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 2013, 30:2725-2729.
68. Turkewitz A.P., Orias E., Kapler G. Functional genomics: the coming of age for Tetrahymena thermophila. Trends Genet. 2002, 18:35-40.
69. Van de Peer Y., Frickey T., Taylor J., Meyer A. Dealing with saturation at the amino acid level: a case study based on anciently duplicated zebrafish genes. Gene 2002, 295:205-211.
70. Xiong, J., Lu, Y., Feng, J., Yuan, D., Tian, M., Chang, Y., Fu, C., Wang, G., Zeng, H., Miao, W., 2013. Tetrahymena functional genomics database (TetraFGD): an integrated resource for Tetrahymena functional genomics. Database (Oxford) 2013, bat008.
71. Yi Z., Song W., Gong J., Warren A., Al-Rasheid K.A.S., Al-Arifi S., Al-Khedhairy A.A. Phylogeny of six oligohymenophoreans (Protozoa, Ciliophora) inferred from small subunit rRNA gene sequences. Zoolog. Scr. 2009, 38:323-331.
72. Zhan Z., Stoeck T., Dunthorn M., Xu K. Identification of the pathogenic ciliate Pseudocohnilembus persalinus (Oligohymenophorea: Scuticociliatia) by fluorescence in situ hybridization. Eur. J. Protistol. 2014, 50:16-24.
73. Zhang Q., Fan X., Clamp J.C., Al-Rasheid K.A., Song W. Description of Paratetrahymena parawassi n. sp. using morphological and molecular evidence and a phylogenetic analysis of Paratetrahymena and other taxonomically ambiguous genera in the order Loxocephalida (Ciliophora, Oligohymenophorea). J. Eukaryot. Microbiol. 2010, 57:483-493.
74. Zhang Q.Q., Yi Z.Z., Fan X.P., Warren A., Gong J., Song W.B. Further insights into the phylogeny of two ciliate classes Nassophorea and Prostomatea (Protista, Ciliophora). Mol. Phylogenet. Evol. 2014, 70:162-170.