Molecular phylogeny, taxonomic relationships and North American distribution of Conchophthirus (Conchophthiridae, Scuticociliatia)

Authors

  • Gregory A. Antipa Department of Biology, San Francisco State University, 1600 Holloway, San Francisco, CA 94132, USA
  • Michaela C. Strüder-Kypke Department of Molecular and Cellular Biology, University of Guelph, Guelph, Ontario N1G 2W1
  • Denis H. Lynn Department of Zoology, University of British Columbia, Vancouver, British Columbia, V6T 1Z4

Keywords:

cytochrome c oxidase subunit 1, SSUrRNA, Anodonta californiensis, Margaritifera falcata

Abstract

Conchophthirus curtus is a scuticociliate found in the mantle cavity of unionid bivalve mussels; it is considered by most to be an endocommensal. It was previously redescribed and its morphogenesis has been carefully defined and evaluated. Conchophthirus stomatogenesis along with its enigmatic deep kinetosomal unit as compared with other scuticociliates, peniculines, and peritrichs suggested possible homologies and affinities. Thus, a comparison of Conchophthirus with common molecular markers to all other ciliates was a goal of this study. We collected Conchophthirus spp. in California from two unionid bivalve hosts: Anodonta californiensis in the Pit River and Lake Merced, and Margaritifera falcata from the Trinity River. The ciliates analyzed were predominantly C. curtus although other conchophthirids were present. The small subunit rRNA and the cytochrome c oxidase subunit 1 genes were sequenced. Phylogenetic analyses of these data were analyzed and maximum likelihood for the small submit rRNA dataset and neighbor-joining for the cytochrome c oxidase subunit 1 dataset. The cytochrome c oxidase subunit 1 sequences obtained from M. falcata populations were virtually identical. The analysis placed these sequences with 96% bootstrap support as sister to Dexiotricha sp. The small submit rRNA sequences obtained from populations from both hosts were almost identical, and they showed them to be sister, with 99% support to two unpublished sequences from Chinese populations of Conchophthirus cucumis and C. lamellidens, and sister to a Dexiotricha sp. These data and their analyses confirm Conchophthirus to be a scuticociliate, but not closely related to either philasterine or pleuronematine scuticociliates nor the peniculines or peritrichs. Further analysis awaits additional data. The North American distribution of Conchophthirus, niche analyses, and potential homologous structures are discussed as well as the use of these endocommensals as indicators of water quality and pollution.

References

Antipa, G.A.

,1971. Structural differentiation in the somatic cortex of a ciliated protozoan, Conchophthirus curtus Engelmann, 1862. Protistologica 4, 471–501. doi:10.1111/j.1550-7408.1997.tb05726.x

Antipa, G.A.

, 1977. Use of commensal protozoa as biological indicators of water quality and pollution. Trans. Am. Microsc. Soc. 96, 482–489. doi:10.2307/3225666

Antipa, G.A.

, 2014. Cellular architecture, growth, morphogenesis, chemoattractants, and loose ends, In:

K Hausmann

,

R. Radek

(Eds.), Cilia and Flagella, Ciliates and Flagellates, pp. 23–45. Schweizerbart, Stuttgart, Germany.

Antipa, G.A.

, Hatzidimitriou, G.

, 1981. Morphogenesis in Conchophthirus curtus: a study of the morphological events associated with binary fission. J. Protozool. 28, 206–14. doi:10.1111/j.1550-7408.1981.tb02834.x

Antipa, G.A.

, Small, E.B.

, 1971a. A redescription of Conchophthirus curtus Engelmann, 1862. J. Protozool. 18, 491–501. doi:10.1111/j.1550-7408.1971.tb03361.x

Antipa, G.A.

, Small, E.B.

, 1971b. The occurrence of thigmotrichous ciliated protozoa inhabiting the mantle cavity of unionid molluscs of Illinois. Trans. Am. Microsc. Soc. 90, 463–72. doi:10.2307/3225461

Antipa, G.A.

, Dolan, J.

, Lynn, D.H.

, Obolkina, L.A.

, Strüder-Kypke, M.C.

, 2016. Molecular phylogeny and evolutionary relationships between the ciliate genera Peniculistoma and Mytilophilus (Peniculistomatidae, Pleuronematida). J. Eukaryot. Microbiol. 63, 642–650. doi:10.1111/jeu.12316

Brown, K.D.

, 1987. Telotroch metamorphosis and stalk morphogenesis in Vorticella striata

. M. A. Thesis, San Francisco State University, San Francisco, CA, USA.

Corliss, J.O.

, 1968. The value of ontogenetic data in reconstructing protozoan phylogenies. Trans. Am. Microsc. Soc. 87, 1–20. doi:10.2307/3224333

Corliss, J.O.

, 1979. The Ciliated Protozoa. Characterization, Classification, and Guide to the Literature. 2nd ed. Pergamon Press, New York, USA.

Darriba, D.

, Taboada, G.L.

, Doallo, R.

, Posada, D.

, 2012. jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772. doi:10.1038/nmeth.2109

Felsenstein, J.

, 2009. PHYLIP (Phylogeny Interference Package) version 3.69. Distributed by the author, Department of Genome Sciences, University of Washington, Seattle, WA. Available at http://evolution.genetics.washington.edu/phylip.html

Fenchel, T.

, 1965. Ciliates from Scandinavian molluscs. Ophelia 2, 71–17. doi:10.1080/00785326.1965.10409598

Fenchel, T.

, 1966. On the ciliated protozoa inhabiting the mantle cavity of lamellibranchs. Malacologica 5, 35–36.

Foissner, W.

, 1996. Ontogenesis in ciliated protozoa with emphasis on stomatogenesis. In:

K. Hausmann

,

P.C. Bradbury

(Eds.), Ciliates: Cells as Organisms, pp. 95–177. Fischer Stuttgart, Jena, Lübeck, Ulm, Germany.

Gao, F.

, Katz, L.A.

, Song, W.

, 2013. Multigene-based analyses on evolutionary phylogeny of two controversial ciliate orders: Pleuronematida and Loxocephalida (Protista, Ciliophora, Oligohymenophorea). Mol. Phylogenet. Evol., 68, 55–63. doi:10.1016/j.ympev.2013.03.018

Jeelani, M.

, Kaur, H.

, Syeed, M.

, Huma, B.

, Sheikh, A.Q.

, Sarwar, S.G.

, 2018. Use of protozoa as biological indicators of water quality and pollution. IJARSE 7, 2021–2030.

Jerome, C.A.

, Simon, E.M

, Lynn, D.H.

, 1996. Description of Tetrahymena empidokyrea n. sp., a new species in the Tetrahymena pyriformis sibling species complex (Ciliophora, Oligohymenophorea), and an assessment of its phylogenetic position using small-subunit rRNA sequences. Can. J. Zool. 74, 1898–1906. doi:10.1139/z96-214

Jones, W.R.

, 1976. Oral morphogenesis during asexual reproduction in Paramecium tetraurelia

. Genet. Res. Camb. 27, 187–204. doi:10.1017/S0016672300016396

Katoh, K.

, Rozewicki, J.

, Yamada, K.D.

, 2017. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief. Bioinform., doi:10.1093/bib/bbx108

Kelly, H.M.

, 1899. A statistical study of the parasites of the Unionidae. Bull. Ill. State Lab. Nat. Hist. 5, 399–418.

Kidder, G.W.

, 1934. Studies on the ciliates from fresh water mussels. I. The structure and neuromotor system of Conchophthirius anodontae Stein, C. curtus Engl., and C. magna sp. nov. Biol. Bull. 66, 69–90. doi:10.2307/1537464

Kimura, M.

, 1980. A simple model for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16, 111–120. doi:10.1007/BF01731581

Kumar, S.

, Stecher, G.

, Tamura, K.

, 2016. MEGA7: Molecular Evolutionary Genetics Analysis version 7 for bigger datasets, Mol. Biol. Evol. 33, 1870–1874. doi:10.1093/molbev/msw054

Lom, J.

, 1964. The morphology and morphogenesis of the buccal ciliary organelles in some peritrichous ciliates. Arch. Protistenkd. 107, 131–162.

Lynn, D. H.

, 2008.

The Ciliated Protozoa: Characterization

, Classification, and Guide to the Literature. 3rd ed. Springer, Dordrecht, NL.

Medlin, L.

, Elwood, H. J.

, Stickel, S.

, Sogin, M.L.

, 1988. The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene. 71, 491–499. doi: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. p. 1–8. In: Proceedings of the Gateway Computing Environments Workshop (GCE), 2010 Nov14, New Orleans, LA.

Peck, R.K.

, 1977. Cortical ultrastructure of the scuticociliates Dexiotricha media and Dexiotricha colpidiopsis (Hymenostomata). J. Protozool., 24, 122–134. doi:10.1111/j.1550-7408.1977.tb05289.x

Penn, J.H.

, 1958. Studies on ciliates from mollusks of Iowa. Proc. Iowa Acad. Set. 65, 517–534.

Penn, O.

, Privman, E.

, Ashkenazy, H.

, Landan, G.

, Graur, D.

, Pupko, T.

, 2010. GUIDANCE: a web server for assessing alignment confidence scores. Nucl. Acids Res., 38, W23–W28; doi:10.1093/nar/gkq44

Raabe, Z.

, 1933. Untersuchungen an Arten des Genus Conchophthirus Stein. (Studies on species of the genus Conchophthirus Stein. In German). Bull. Int. Acad. Cracovie (Acad. Pol. Sci.), (B. 2) 1932, 295–310.

Raabe, Z.

, 1971. Ordo Thigmotricha (Ciliata-Holotricha). IV. Familia Thigmophryidae. (Order Thigmotrichia (Ciliata-Holotricha). IV. Family Thigmophryidae. In German). Acta Protozool. 9, 121–170.

Rataj, M.

, Vd’ačný, P.

, 2018. Dawn of astome ciliates in light of morphology and time-calibrated phylogeny of Haptophrya planarium, an obligate endosymbiont of freshwater turbellarians. Europ. J. Protistol. 64, 54–71. doi:10.1016/j.ejop.2018.03.004

Ronquist, F.

, Teslenko, M.

, van der Mark, P.

, Ayres, D.L.

, Darling, A.

, Höhna, S.

, Larget, B.

, Liu, L.

, Suchard, M.A.

, Huelsenbeck, J.P.

, 2012. MRBAYES 3.2: Efficient Bayesian phylogenetic inference and model selection across a large model space. Syst. Biol. 61, 539–542. doi:10.1093/sysbio/sys029

Saitou, N.

, Nei, M.

, 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406–425. doi:10.1093/oxfordjournals.molbev.a040454

Sela, I.

, Ashkenazy, H.

, Katoh, K.

, Pupko, T.

, 2015. GUIDANCE2: accurate detection of unreliable alignment regions accounting for the uncertainty of multiple parameters. Nucl. Acids Res., 43: W7–W14.; doi:10.1093/nar/gkq443

Small, E.B.

, 1967. The Scuticociliatida, a new order of the class Ciliatea (phylum Protozoa, subphylum Ciliophora). Trans. Am. Microsc. Soc. 86, 345–370. doi:10.2307/3224258

Stamatakis, A

, Hoover, P.

, Rougemont, J.

, 2008. A rapid bootstrap algorithm for the RAxML Web-Servers. Syst. Biol. 75, 758–771. doi:10.1080/10635150802429642

Strüder-Kypke, M.C.

, Lynn, D.H.

, 2010. Comparative analysis of the mitochondrial cytochrome c oxidase subunit I (COI) gene in ciliates (Alveolata, Ciliophora) and evaluation of its suitability as a biodiversity marker. Syst. Biodivers. 8, 131–148. doi:10.1080/14772000903507744

Wilbur, C.G.

, 1969.

The Biological Aspects of Water Pollution

. Charles C. Thomas, Springfield.

Zhang, T.

, Fan, X.

, Gao, F.

, Al-Farraj, S.A.

, El-Serehy, H.A.

, Song, W.

, 2019. Further analyses on the phylogeny of the subclass Scuticociliatia (Protozoa,Ciliophora) based on both nuclear and mitochondrial data. Mol. Phylogenet. Evol. 139, 1–11.

Published

2020-01-02