Cite this paper:
CAI Xinglong, CHEN Ying, ZHAO Xiaolu, GAO Jing, Saleh A. AL-FARRAJ, YU Lijie, PAN Xuming, QIU Zijian. Molecular phylogeny and ultrastructure of a new population of Urostyla grandis (Ciliophora, Hypotrichida) from Harbin, China[J]. Journal of Oceanology and Limnology, 2019, 37(1): 256-265

Molecular phylogeny and ultrastructure of a new population of Urostyla grandis (Ciliophora, Hypotrichida) from Harbin, China

CAI Xinglong1, CHEN Ying1, ZHAO Xiaolu2, GAO Jing1, Saleh A. AL-FARRAJ3, YU Lijie1, PAN Xuming1, QIU Zijian1
1 Laboratory of Protozoology, Harbin Normal University, Harbin 150025, China;
2 Institute of Evolution & Marine Biodiversity, Ocean University of China, Qingdao 266003, China;
3 Zoology Department, College of Science, King Saud University, Riyadh 11451, Saudi Arabia
Abstract:
A new population of Urostyla grandis, collected from a freshwater pond of northeastern China was investigated by living observation, silver impregnation, and molecular phylogeny based on small subunit ribosomal rRNA (SSU rRNA). Besides, its ultrastructural characteristics were investigated carefully by scanning electron microscopy (SEM) and transmission electron microscopy (TEM) methods. Complementary descriptions of some inner ultrastructures were provided and some new organelles were also found. Especially, the oral inner microtubule system was illustrated by SEM and TEM for the first time and a new type extrusome was reported. These results may supply complement taxonomic data and ingestion mechanism on ciliates in genus Urostyla.
Key words:    Urostyla grandis|phylogeny|ultrastructure|new population   
Received: 2017-10-03   Revised: 2017-12-29
Tools
PDF (1836 KB) Free
Print this page
Add to favorites
Email this article to others
Authors
Articles by CAI Xinglong
Articles by CHEN Ying
Articles by ZHAO Xiaolu
Articles by GAO Jing
Articles by Saleh A. AL-FARRAJ
Articles by YU Lijie
Articles by PAN Xuming
Articles by QIU Zijian
References:
Aescht E. 2001. Catalogue of the generic names of ciliates(Protozoa, Ciliophora). Denisia, 1:1-350.
Alekperov I K. 1984. New freshwater ciliates (Hypotrichida)from water bodies of Azerbaijan. Zoologicheskiĭ zhurnal, 63:1 458-1 463. (in Russian with English abstract)
Allen R D, Staehelin L A. 1981. Digestive system membranes:freeze-fracture evidence for differentiation and flow in Paramecium. The Journal of Cell Biology, 89(1):9-20.
Bardele C F. 1981. Functional and phylogenetic aspects of the ciliary membrane:a comparative freeze-fracture study.Biosystems, 14(3-4):403-421, https://doi.org/10.1016/0303-2647(81)90046-0.
Berger H. 2001. Catalogue of Ciliate Names 1. Hypotrichs.Verlag Helmut Berger, Salzburg. 206p.
Berger H. 2006. Monograph of the Urostyloidea (Ciliophora, Hypotricha). Springer, Dordrecht. p.1-1 303.
Borror A C. 1972. Revision of the order Hypotrichida(Ciliophora, Protozoa). The Journal of Protozoology, 19(1):1-23, https://doi.org/10.1111/j.1550-7408.1972.tb03407.x.
Borror A C. 1979. Redefinition of the Urostylidae (Ciliophora, Hypotrichida) on the basis of morphogenetic characters.The Journal of Protozoology, 26(4):544-550, https://doi.org/10.1111/j.1550-7408.1979.tb04192.x.
Chorik F P. 1968. Free-living Ciliates in Moldavian Water Basins. Akadmia Nauk MSSR, Kischinev. 251p. (in Russian)
Croft K E, Dalby A B, Hogan D J, Orr K E, Hewitt E A, Africa R J, DuBois M L, Prescott D M. 2003. Macronuclear molecules encoding actins in spirotrichs. Journal of Molecular Evolution, 56(3):341-350, https://doi.org/10.1007/s00239-002-2405-2.
Dalby A B, Prescott D M. 2004. The scrambled actin I gene in Uroleptus pisces. Chromosoma, 112(5):247-254, https://doi.org/10.1007/s00412-003-0270-4.
Ehrenberg C G. 1832a. Beiträge zur kenntniss der organisation der infusorien und ihrer geographischen verbreitung, besonders in Sibirien. Abhandlungen der Preussischen Akademie der Wissenschaften, 1830:1-88.
Ehrenberg C G. 1832b. Űber die entwickelung und lebensdauer der infusionsthiere; nebst ferneren Beiträgen zu einer Vergleichung ihrer organischen Systeme. Abhandlungen der Königlichen Akademie Wissenschaften zu Berlin, Physikalische Klasse, 1831:1-154.
Ehrenberg C G. 1838. Die Infusionsthierchen als Vollkommene Organismen-Ein Blick in das Tiefere Organische Leben der Natur. Leopold Voss, Leipzig. 548p.
Ganner B. 1991. Zur Taxonomie einiger Ciliaten (Protozoa)aus Fliessgewässern. Dissertation Universität Salzburg. 159p.
Gao J, Zhou W, Qiao L, Chen Y, Qiu Z J. 2011. A new method of sample preparation for scanning electron microscope used to observe the structure under pellicle in ciliates.Chinese Journal of Cell Biology, 33(9):1 004-1 007. (in Chinese with English abstract)
Gong J, Stoeck T, Yi Z Z, Miao M, Zhang Q Q, Roberts D M, Warren A, Song W B. 2009. Small subunit rRNA phylogenies show that the class Nassophorea is not monophyletic (Phylum Ciliophora). Journal of Eukaryotic Microbiology, 56(4):339-347, https://doi.org/10.1111/j.1550-7408.2009.00413.x.
Gu F K, Chen L, Ni B, Zhang X M. 2002. A comparative study on the electron microscopic enzymo-cytochemistry of Paramecium bursaria from light and dark cultures.European Journal of Protistology, 38(3):267-278, https://doi.org/10.1078/0932-4739-00875.
Hall T A. 1999. BioEdit:a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41:95-98.
Hewitt E A, Müller K M, Cannone J, Hogan D J, Gutell R, Prescott D M. 2003. Phylogenetic relationships among 28 spirotrichous ciliates documented by rDNA. Molecular Phylogenetics and Evolution, 29(2):258-267, https://doi.org/10.1016/S1055-7903(03)00097-6.
Hoffman D C, Prescott D M. 1997. Phylogenetic relationships among hypotrichous ciliates determined with the macronuclear gene encoding the large, catalytic subunit of DNA polymerase α. Journal of Molecular Evolution, 45(3):301-310, https://doi.org/10.1007/PL00006234.
Inaba F, Suganuma Y. 1966. Electron microscopy of the nuclear apparatus of urostyla grandis, a Hypotrichous ciliate. The Journal of Protozoology, 13(1):137-143, https://doi.org/10.1111/j.1550-7408.1966.tb01884.x.
Jankowski A W. 1979. Revision of the order Hypotrichida Stein, 1859. Generic catalogue, phylogeny, taxonomy.Academy of Science USSR, Proceedings of the Zoological Institute, 86:48-85. (in Russian with English abstract)
Jerka-Dziadosz M. 1963. Morphogenesis in division and regeneration of Urostyla grandis Ehrbg. Acta Protozool, 1:43-54.
Jerka-Dziadosz M. 1972. Cortical development in Urostyla. I.comparative study on morphogenesis in U. cristata and U.grandis. Acta Protozool, 10:73-100.
Kahl A. 1932. Urtiere oder Protozoa I:Wimpertiere oder Ciliata (Infusoria) 3. Spirotricha. Tierwelt Dtl, 25:399-650.
Kumar S, Nei M, Dudley J, Tamura K. 2008. MEGA:a biologist-centric software for evolutionary analysis of DNA and protein sequences. Briefings in Bioinformatics, 9(4):299-306, https://doi.org/10.1093/bib/bbn017.
Li Y S, Niu Y N, Liu L X. 2008. Phylogenetic studies of four species of ciliate inferred from 16s-like small subunit rRNA gene sequences. Journal of Forestry Research, 19(2):119-124, https://doi.org/10.1007/s11676-008-0020-9.
Lundin F C, West L S. 1963. The Free-living Protozoa of the Upper Peninsula of Michigan ([Northern Michigan College] Monographic series). Northern Michigan College Press, Marquette. 175p.
Lynn D H. 2008. The Ciliated Protozoa:Characterization, Classification, and Guide to the Literature. 3rd edn.Springer, Dordrecht. p.1-605.
Medlin L, Elwood H J, Stickel S, Sogin M L. 1988. The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene, 71(2):491-499, https://doi.org/10.1016/0378-1119(88)90066-2.
Miller M A, Pfeiffer W, Schwartz T. 2010. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In:Proceedings of 2010 Gateway Computing Environments Workshop. IEEE, New Orleans, LA. p.1-8, https://doi.org/10.1109/GCE.2010.5676129.
Nylander J A A. 2004. MrModeltest Version 2. Program Distributed by the Author. Uppsala University, Uppsala.
Penn O, Privman E, Ashkenazy H, Landan G, Graur D, Pupko T. 2010b. GUIDANCE:a web server for assessing alignment confidence scores. Nucleic Acids Research, 38(S2):W23-W28, https://doi.org/10.1093/nar/gkq443.
Penn O, Privman E, Landan G, Graur D, Pupko T. 2010a. An alignment confidence score capturing robustness to guide tree uncertainty. Molecular Biology and Evolution, 27(8):1 759-1 767, https://doi.org/10.1093/molbev/msq066.
Preisig H R, Anderson O R, Corliss J O, Moestrup Ø, Powell M J, Roberson R W, Wetherbee R. 1994. Terminology and nomenclature of protist cell surface structures.Protoplasma, 181(1-4):1-28, https://doi.org/10.1007/BF01666386.
Reuter J. 1961. Einige faunistische und ökologische Beobachtungen über Felsentümpel-Ziliaten. Acta zoologica Fennica, 99:1-42.
Ronquist F, Huelsenbeck J P. 2003. MRBAYES 3:Bayesian phylogenetic inference under mixed models.Bioinformatics, 19(12):1 572-1 574, https://doi.org/10.1093/bioinformatics/btg180.
Rosati G, Modeo L. 2003. Extrusomes in ciliates:diversification, distribution, and phylogenetic implications. The Journal of Eukaryotic Microbiology, 50(6):383-402, https://doi.org/10.1111/j.1550-7408.2003.tb00260.x.
Ruthmann A, Noll-Altmann G. 1980. Effect of bacterial symbiont on cell division in a ciliate. In:Schwemmler W, Schenk H E A eds. Endocytobiology:Endosymbiosis and Cell Biology Volume 1. Walter de Gruyter & Co, Berlin, New York. p.361-370.
Sattler C A, Staehelin L A. 1976. Reconstruction of oral cavity of Tetrahymena pyriformis utilizing high voltage electron microscopy. Tissue and Cell, 8(1):1-18, https://doi.org/10.1016/0040-8166(76)90016-1.
Sattler C A, Staehelin L A. 1979. Oral cavity of Tetrahymena pyriformis:a freeze-fracture and high-voltage electron microscopy study of the oral ribs, cytostome, and forming food vacuole. Journal of Ultrastructure Research, 66(2):132-150, https://doi.org/10.1016/S0022-5320(79)90130-8.
Shi X B, Frankel J. 1990. Morphology and development of Mirror-Image doublets of Stylonychia mytilus. The Journal of Protozoology, 37(1):1-13, https://doi.org/10.1111/j.1550-7408.1990.tb01106.x.
Shin M K. 1994. Systematics of Korean Hypotrichs(Ciliophora, Polyhymenophora, Hypotrichida) and Molecular Evolution of Hypotrichs. Seoul National University, Seoul. 270p.
Smith H E. 1982. Oral apparatus structure in the carnivorous macrostomal form of Tetrahymena vorax. The Journal of Protozoology, 29(4):616-627, https://doi.org/10.1111/j.1550-7408.1982.tb01348.x.
Smith-Somerville H E, Buhse Jr H E. 1984. Changes in oral apparatus structure accompanying vacuolar formation in the macrostomal form of Tetrahymena vorax. A model for the formation of food vacuoles in Tetrahymena. The Journal of Protozoology, 31(3):373-380, https://doi.org/10.1111/j.1550-7408.1984.tb02982.x.
Song W B, Wilbert N. 1989. Taxonomische untersuchungen an aufwuchsciliaten (protozoa, ciliophora) im poppelsdorfer weiher, Bonn. Lauterbornia, Heft, 3:2-221.
Stamatakis A, Hoover P, Rougemont J. 2008. A rapid bootstrap algorithm for the RAxML web servers. Systematic Biology, 57(5):758-771, https://doi.org/10.1080/10635150802429642.
Stamatakis A. 2006. RAxML-VI-HPC:maximum likelihoodbased phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22(21):2 688-2 690, https://doi.org/10.1093/bioinformatics/btl446.
Stein F. 1859. Der Organismus der Infusionsthiere Nach Eigenen Forschungen in Systematischer Reihenfolge Bearbeitet. I. Engelmann, Leipzig. 206p.
Stokes A C. 1885. XL.-Some new infusoria from American fresh waters. Annals and Magazine of Natural History:Series 5, 15(90):437-449, https://doi.org/10.1080/00222938509459365.
Stokes A C. 1886. Some new Hypotrichous infusoria.Proceedings of the American Philosophical Society, 23(121):21-30.
Stokes A C. 1891. Notes of new infusoria from the fresh waters of the United States. Journal of the Royal Microscopical Society, 11(6):697-704, https://doi.org/10.1111/j.1365-2818.1891.tb01611.x.
Suganuma Y, Inaba F. 1966. Electron microscopy of the macronucleus in interphase of Urostyla grandis.Doubutsugaku Zasshi, 75(6):172-177. (in Japanese with English abstract)
Suganuma Y, Inaba F. 1967. Electron microscopic study of the macronuclei of Urostyla grandis during binary fission.Zoological magazine, 76(4):110-118.
Sui S G, Chen Y, Qiu Z J, Shi X B. 2001. Structure of oral apparatus in Stylonychia mytilus. Acta Zoologica Sinica, 47(4):436-441. (in Chinese with English abstract)
Wang C C. 1925. Study of the protozoa of Nanking Part I.Contr. Boil. Lab. Sci. Soc. China, 1:1-60.
Zhang J, Ni B, Sheng C, Gu F K. 2007. Observations on the ultrastructure of mucocyst in Urostyla grandis. Journal of Fudan University (Natural Science), 46(6):972-975. (in Chinese with English abstract)
Zhao L, Li Y S, Li J G, Gu F K. 2009. Some ultrastructural observations of the vegetative, resting and excysting ciliate, urostyla grandis (urostylidae, hypotrichida).Biological Research, 42(4):395-401, https://doi.org/10.4067/S0716-97602009000400001.
Copyright © Haiyang Xuebao