Santoferrara, L.F.; Alder, V.V.; McManus, G.B."Phylogeny, classification and diversity of Choreotrichia and Oligotrichia (Ciliophora, Spirotrichea)" (2017) Molecular Phylogenetics and Evolution. 112:12-22
Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor


Ciliated protists in the subclasses Choreotrichia and Oligotrichia are major components of marine plankton. Despite their ecological relevance, there are uncertainties in their systematics and diversity. We retrieved and curated all the GenBank ribosomal DNA (rDNA) sequences from these groups, which were analyzed in two ways. The first approach was based on morphologically-identified sequences (including those of two families and six genera newly studied here by single-cell sequencing), and aimed at improving phylogenetic inferences using concatenated sequences of three rDNA loci. Based on phylogenetic and morphological support, we update the taxonomic classification of these subclasses into 23 families, including the re-established Favellidae. We also propose an informal naming system for incertae sedis taxa, namely Tintinnopsis and five related genera that are spread among eleven lineages. The second approach included unidentified environmental sequences, and was used to explore potentially novel diversity in these subclasses. Our results support high proportions of both synonyms in tintinnids and uncharacterized taxa in choreotrichids and oligotrichs. One previously unidentified, environmental clade is here linked to our new Leegaardiellidae sequences. Our curation of almost 4000 rDNA sequences exemplifies known issues of public repositories, and suggests caution in both the use and contribution to these unique resources for evolutionary and diversity studies. © 2017 Elsevier Inc.


Documento: Artículo
Título:Phylogeny, classification and diversity of Choreotrichia and Oligotrichia (Ciliophora, Spirotrichea)
Autor:Santoferrara, L.F.; Alder, V.V.; McManus, G.B.
Filiación:Department of Marine Sciences, University of Connecticut, Groton, CT 06340, United States
Instituto de Ecología, Genética y Evolución de Buenos Aires (UBA-CONICET) y Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, C1428EHA, Argentina
Instituto Antártico Argentino, Dirección Nacional del Antártico, Buenos Aires, C1010AAZ, Argentina
Palabras clave:Ciliate; Environmental sequencing; Protist; Sequence curation; Single-cell sequencing; Tintinnid; protozoal DNA; ribosome DNA; biodiversity; ciliate; classification; DNA sequence; evolution; genetics; phylogeny; plankton; Biodiversity; Biological Evolution; Ciliophora; DNA, Protozoan; DNA, Ribosomal; Phylogeny; Plankton; Sequence Analysis, DNA
Página de inicio:12
Página de fin:22
Título revista:Molecular Phylogenetics and Evolution
Título revista abreviado:Mol. Phylogenet. Evol.
CAS:DNA, Protozoan; DNA, Ribosomal


  • Agatha, S., Evolution of ciliary patterns in the Oligotrichida (Ciliophora, Spirotricha) and its taxonomic implications (2004) Zoology, 107, pp. 153-168
  • Agatha, S., Redescription of Tintinnopsis parvula Jörgensen, 1912 (Ciliophora: Spirotrichea: Tintinnina), including a novel lorica matrix (2010) Acta Protozool., 49, pp. 213-234
  • Agatha, S., Global diversity of aloricate Oligotrichea (Protista, Ciliophora, Spirotricha) in marine and brackish sea water (2011) PLoS One, 6, p. e22466
  • Agatha, S., Strüder-Kypke, M.C., Reconciling cladistic and genetic analyses in Choreotrichid Ciliates (Ciliophora, Spirotricha, Oligotrichea) (2012) J. Eukaryot. Microbiol., 59, pp. 325-350
  • Agatha, S., Laval-Peuto, M., Simon, P., The tintinnid lorica (2013) The Biology and Ecology of Tintinnid Ciliates: Models for Marine Plankton, pp. 17-41. , J.R. Dolan D.J.S. Montagnes S. Agatha D.W. Coats D.K. Stoecker Wiley-Blackwell Oxford
  • Agatha, S., Strüder-Kypke, M.C., Systematics and evolution of tintinnid ciliates (2013) The Biology and Ecology of Tintinnid Ciliates: Models for Marine Plankton, pp. 42-84. , J.R. Dolan D.J.S. Montagnes S. Agatha D.W. Coats D.K. Stoecker Wiley-Blackwell Oxford
  • Agatha, S., Strüder-Kypke, M.C., What morphology and molecules tell us about the evolution of Oligotrichea (Alveolata, Ciliophora) (2014) Acta Protozool., 53, pp. 77-90
  • Alder, V.A., Tintinnoinea (1999) South Atlantic Zooplankton, pp. 321-384. , D. Boltovskoy Backhuys Publishers Leiden
  • Bachy, C., Gómez, F., López-García, P., Dolan, J.R., Moreira, D., Molecular phylogeny of tintinnid ciliates (Tintinnida, Ciliophora) (2012) Protist, 163, pp. 873-887
  • Bachy, C., Dolan, J.R., Lopez-Garcia, P., Deschamps, P., Moreira, D., Accuracy of protist diversity assessments: morphology compared with cloning and direct pyrosequencing of 18S rRNA genes and ITS regions using the conspicuous tintinnid ciliates as a case study (2013) ISME J., 7, pp. 244-255
  • Bakker, C., Phaff, W.J., Tintinnida from coastal waters of the S. W. Netherlands 1. The genus Tintinnopsis Stein (1976) Hydrobiologia, 50, pp. 101-111
  • Balech, E., Algunas especies nuevas o interesantes de tintinnidos del Golfo de México y Caribe. Revista del Museo Argentino de Ciencias Naturales Bernardino Rivadavia (1968) Hidrobiología, 2, pp. 165-197
  • Calbet, A., Saiz, E., The ciliate-copepod link in marine ecosystems (2005) Aquat. Microb. Ecol., 38, pp. 157-167
  • Camacho, C., Coulouris, G., Avagyan, V., Ma, N., Papadopoulos, J., Bealer, K., Madden, T., BLAST+: architecture and applications (2009) BMC Bioinf., 10, p. 421
  • Campbell, A., Tintinnina. Protista 3 (1954) Treatise on Invertebrate Paleontology, pp. 166-180. , A. Campbell R.C. Moore Kansas University Press Lawrence
  • Capella-Gutiérrez, S., Silla-Martínez, J.M., Gabaldón, T., TrimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses (2009) Bioinformatics, 25, pp. 1972-1973
  • Castresana, J., Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis (2000) Mol. Biol. Evol., 17, pp. 540-552
  • Corliss, J.O., Biodiversity and biocomplexity of the protists and an overview of their significant roles in maintenance of our biosphere (2002) Acta Protozool., 41, pp. 199-219
  • Cotterill, F., Al-Rasheid, K., Foissner, W., Conservation of protists: is it needed at all? (2008) Biodiv. Conserv., 17, pp. 427-443
  • Doherty, M., Costas, B., McManus, G., Katz, L., Culture-independent assessment of planktonic ciliates in coastal northwest Atlantic waters (2007) Aquat. Microb. Ecol., 48, pp. 141-154
  • Dolan, J.R., Planktonic protists: little bugs pose big problems for biodiversity assessments (2016) J. Plankton Res., 38, pp. 1044-1051
  • Dolan, J.R., Pierce, R.W., Diversity and distributions of tintinnids (2013) The Biology and Ecology of Tintinnid Ciliates: Models for Marine Plankton, pp. 214-243. , J.R. Dolan D.J.S. Montagnes S. Agatha D.W. Coats D.K. Stoecker Wiley-Blackwell Oxford
  • Dunthorn, M., Otto, J., Berger, S., Stamatakis, A., Mahé, F., Placing environmental next generation sequencing amplicons from microbial eukaryotes into a phylogenetic context (2014) Mol. Biol. Evol., 31, pp. 993-1009
  • Edgar, R.C., Search and clustering orders of magnitude faster than BLAST (2010) Bioinformatics, 26, pp. 2460-2461
  • Edgar, R.C., Haas, B.J., Clemente, J.C., Quince, C., Knight, R., UCHIME improves sensitivity and speed of chimera detection (2011) Bioinformatics, 27, pp. 2194-2200
  • Forster, D., Bittner, L., Karkar, S., Dunthorn, M., Romac, S., Testing ecological theories with sequence similarity networks: marine ciliates exhibit similar geographic dispersal patterns as multicellular organisms (2015) BMC Biol., 13, p. 16
  • Gimmler, A., Korn, R., de Vargas, C., Audic, S., Stoeck, T., The Tara Oceans voyage reveals global diversity and distribution patterns of marine planktonic ciliates (2016) Sci. Rep., 6, p. 33555
  • Grattepanche, J.-D., Santoferrara, L.F., McManus, G.B., Katz, L.A., Unexpected biodiversity of ciliates in marine samples from below the photic zone (2016) Mol. Ecol., 25, pp. 3987-4000
  • Hofer, U., Marine microbiology: changing climate, changing plankton communities (2016) Nat. Rev. Micro., 14, p. 2
  • Jörgensen, E., Mediterranean tintinnids (1924), Report on the Danish Oceanographical Expeditions 1908–10 to the Mediterranean and adjacent Seas. 2 J.3. Biology, pp. 1–110; Katoh, K., Standley, D., MAFFT multiple sequence alignment software version 7: improvements in performance and usability (2013) Mol. Biol. Evol., 30, pp. 772-780
  • Katz, L.A., McManus, G.B., Snoeyenbos-West, O., Griffin, A., Pirog, K., Reframing the ‘Everything is everywhere’ debate: evidence for high gene flow and diversity in ciliate morphospecies (2005) Aquat. Microb. Ecol., 41, pp. 55-65
  • Kim, S.Y., Yang, E.J., Gong, J., Choi, J.K., Redescription of Favella ehrenbergii (Claparède and Lachmann, 1858) Jörgensen, 1924 (Ciliophora: Choreotrichia), with phylogenetic analyses based on small subunit rRNA gene sequences (2010) J. Eukaryot. Microbiol., 57, pp. 460-467
  • Kim, S.Y., Choi, J.K., Dolan, J.R., Shin, H.C., Lee, S., Morphological and ribosomal DNA-based characterization of six Antarctic ciliate morphospecies from the Amundsen Sea with phylogenetic analyses (2013) J. Eukaryot. Microbiol., 60, pp. 497-513
  • Kofoid, C., Campbell, A., A Conspectus of the Marine and Freshwater Ciliata Belonging to the Suborder Tintinnoinea, With Description of New Species Principally From the Agassiz Expedition to the Eastern Tropical Pacific 1904–1905 (1929), University of California Press Berkeley; Kozlov, A.M., Zhang, J., Yilmaz, P., Glöckner, F.O., Stamatakis, A., Phylogeny-aware identification and correction of taxonomically mislabeled sequences (2016) Nucleic Acids Res., 44, pp. 5022-5033
  • Lackey, J.B., Balech, E., A new marine tintinnid (1966) Trans. Am. Microsc. Soc., 85, pp. 575-578
  • Laval-Peuto, M., Construction of the lorica in Ciliata Tintinnina in vivo study of Favella ehrenbergii: variability of the phenotypes during the cycle, biology, statistics, biometry (1981) Protistologica, 17, pp. 249-272
  • Laval-Peuto, M., Classe des Oligotrichea Bütschli, 1887. Ordre des Tintinnida Kofoid et Campbell, 1929 (1994) Traité de Zoologie Anatomie, Systématique, Biologie II Infusoires Ciliés 2 Systématique, pp. 181-219. , P. de Puytorac Masson Paris, Milan
  • Laval-Peuto, M., Barria de Cao, M.S., Les capsules, extrusomes caracteristiques des Tintinnina (Ciliophora) (1987) permettent une classification evolutive des genres et des familles du sous-ordre., pp. 53-60. , Ile Réun. Scientif. GRECO 88, Trav. C.R.M. 8
  • Lie, A., Liu, Z., Hu, S., Jones, A., Kim, D., Investigating microbial eukaryotic diversity from a global census: Insights from a comparison of pyrotag and full-length sequences of 18S rRNA genes (2014) Appl. Environ. Microbiol., 80, pp. 4363-4373
  • Liu, W., Yi, Z., Lin, X., Al-Rasheid, K.A.S., Morphologic and molecular data suggest that Lynnella semiglobulosa n. g., n. sp. represents a new family within the subclass Choreotrichia (Ciliophora, Spirotrichea) (2011) J. Eukaryot. Microbiol., 58, pp. 43-49
  • Liu, W., Yi, Z., Xu, D., Clamp, J.C., Li, J., Two new genera of planktonic ciliates and insights into the evolution of the family Strombidiidae (Protista, Ciliophora, Oligotrichia) (2015) PLoS One, 10, p. e0131726
  • Liu, W., Xu, D., Ma, H., Al-Farraj, S.A., Warren, A., Taxonomy and molecular systematics of three oligotrich (s.l.) ciliates including descriptions of two new species, Strombidium guangdongense sp. nov. and Strombidinopsis sinicum sp. nov. (Protozoa, Ciliophora) (2016) Syst. Biodiv., pp. 1-14
  • Lynn, D.H., The Ciliated Protozoa. Characterization, Classification, and Guide to the Literature (2008), Springer Verlag Dordrecht; Marshall, S.M., Protozoa, order Tintinnia (1969) Conseil International pour l'Exploration de la Mer, Fiches d'Identification de Zooplancton, fiches, pp. 117-127
  • McManus, G.B., Xu, D., Costas, B.A., Katz, L.A., Genetic identities of cryptic species in the Strombidium stylifer/apolatum/oculatum cluster, including a description of Strombidium rassoulzadegani n. sp (2010) J. Eukaryot. Microbiol., 57, pp. 369-378
  • McManus, G.B., Santoferrara, L.F., Tintinnids in microzooplankton communities (2013) Biology and Ecology of Tintinnid Ciliates: Models for Marine Plankton, pp. 198-213. , J.R. Dolan S. Agatha D.W.C. Coats D.J.S. Montagnes D.K. Stoecker Wiley-Blackwell Oxford
  • Morard, R., Escarguel, G., Weiner, A.K.M., André, A., Douady, C.J., Nomenclature for the nameless: a proposal for an integrative molecular taxonomy of cryptic diversity exemplified by planktonic Foraminifera (2016) Syst. Biol., 65, pp. 925-940
  • Nylander, J.A.A., MrModeltest v2. Program distributed by the author (2004), Evolutionary Biology Centre, Uppsala University Sweden; Pfenninger, M., Bálint, M., Pauls, S.U., Methodological framework for projecting the potential loss of intraspecific genetic diversity due to global climate change (2012) BMC Evolutionary Biol., 12, p. 224
  • Pierce, R.W., Turner, J.T., Ecology of planktonic ciliates in marine food webs (1992) Rev. Aquat. Sci., 6, pp. 139-181
  • Price, M.N., Dehal, P.S., Arkin, A.P., FastTree 2 – approximately maximum-likelihood trees for large alignments (2010) PLoS One, 5, p. e9490
  • Pyron, R.A., Burbrink, F.T., Phylogenetic estimates of speciation and extinction rates for testing ecological and evolutionary hypotheses (2013) Trends Ecol. Evol., 28, pp. 729-736
  • Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space (2012) Syst. Biol., 61, pp. 539-542
  • Sanders, R.W., Wickham, S.A., Planktonic protozoa and metazoa: predation, food quality and population control (1993) Mar. Microb. Food Webs, 7, pp. 197-223
  • Santoferrara, L.F., Alder, V.A., Morphological variability, spatial distribution and abundance of Helicostomella species (Ciliophora, Tintinnina) in relation to environmental factors (Argentine shelf; 40–55°S) (2009) Sci. Mar., 73, pp. 701-716
  • Santoferrara, L.F., McManus, G.B., Alder, V.A., Phylogeny of the order Tintinnida (Ciliophora, Spirotrichea) inferred from small- and large-subunit rRNA genes (2012) J. Eukaryot. Microbiol., 59, pp. 423-426
  • Santoferrara, L.F., McManus, G.B., Alder, V.A., Utility of genetic markers and morphology for species discrimination within the order Tintinnida (Ciliophora, Spirotrichea) (2013) Protist, 164, pp. 24-36
  • Santoferrara, L.F., Grattepanche, J.-D., Katz, L.A., McManus, G.B., Pyrosequencing for assessing diversity of eukaryotic microbes: analysis of data on marine planktonic ciliates and comparison with traditional methods (2014) Env. Microbiol., 16, pp. 2752-2763
  • Santoferrara, L.F., Tian, M., Alder, V.A., McManus, G.B., Discrimination of closely related species in tintinnid ciliates: new insights on crypticity and polymorphism in the genus Helicostomella (2015) Protist, 166, pp. 78-92
  • Santoferrara, L.F., Grattepanche, J.-D., Katz, L.A., McManus, G.B., Patterns and processes in microbial biogeography: do molecules and morphologies give the same answers? (2016) ISME J., 10, pp. 1779-1790
  • Santoferrara, L.F., Bachy, C., Alder, V.A., Gong, J., Kim, Y.-O., Updating biodiversity studies in loricate protists: the vase of the tintinnids (Alveolata, Ciliophora, Spirotrichea) (2016) J. Eukaryot. Microbiol., 63, pp. 651-656
  • Snoeyenbos-West, O., Salcedo, T., McManus, G., Katz, L., Insights into the diversity of choreotrich and oligotrich ciliates (Class: Spirotrichea) based on genealogical analyses of multiple loci (2002) Int. J. Syst. Evol. Microbiol., 52, pp. 1901-1913
  • Stamatakis, A., RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies (2014) Bioinformatics, 30, pp. 1312-1313
  • Stoeck, T., Taylor, G., Epstein, S., Novel eukaryotes from the permanently anoxic Cariaco Basin (Caribbean Sea) (2003) Appl. Environ. Microbiol., 69, pp. 5656-5663
  • Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods (2011) Mol. Biol. Evol., 28, pp. 2731-2739
  • Tsai, S.-F., Chen, W.-T., Chiang, K.-P., Phylogenetic position of the genus Cyrtostrombidium, with a description of Cyrtostrombidium paralongisomum nov. spec. and a redescription of Cyrtostrombidium longisomum Lynn & Gilron, 1993 (Protozoa, Ciliophora) based on live observation, protargol impregnation, and 18S rDNA sequences (2015) J. Eukaryot. Microbiol., 62, pp. 239-248
  • Vamosi, S.M., Heard, S.B., Vamosi, J.C., Webb, C.O., Emerging patterns in the comparative analysis of phylogenetic community structure (2009) Mol. Ecol., 18, pp. 572-592
  • Xu, D., Sun, P., Shin, M.K., Kim, Y.O.K., Species boundaries in tintinnid ciliates: A case study – morphometric variability, molecular characterization, and temporal distribution of Helicostomella species (Ciliophora, Tintinnina) (2012) J. Eukaryot. Microbiol., 59, pp. 351-358
  • Xu, D., Sun, P., Warren, A., Hoon, N.J., Lim, C.D., Phylogenetic investigations on ten genera of tintinnid ciliates (Ciliophora: Spirotrichea: Tintinnida), based on small subunit ribosomal RNA gene sequences (2013) J. Eukaryot. Microbiol., 60, pp. 192-202
  • Yi, Z., Strüder-Kypke, M., Hu, X., Lin, X., Song, W., Sampling strategies for improving tree accuracy and phylogenetic analyses: a case study in ciliate protists, with notes on the genus Paramecium (2014) Mol. Phylog. Evol., 71, pp. 142-148
  • Zhang, Q., Agatha, S., Zhang, W., Dong, J., Yu, Y., Three rDNA loci-based phylogenies of tintinnid ciliates (Ciliophora, Spirotrichea, Choreotrichida) (2016) J. Eukaryot. Microbiol.


---------- APA ----------
Santoferrara, L.F., Alder, V.V. & McManus, G.B. (2017) . Phylogeny, classification and diversity of Choreotrichia and Oligotrichia (Ciliophora, Spirotrichea). Molecular Phylogenetics and Evolution, 112, 12-22.
---------- CHICAGO ----------
Santoferrara, L.F., Alder, V.V., McManus, G.B. "Phylogeny, classification and diversity of Choreotrichia and Oligotrichia (Ciliophora, Spirotrichea)" . Molecular Phylogenetics and Evolution 112 (2017) : 12-22.
---------- MLA ----------
Santoferrara, L.F., Alder, V.V., McManus, G.B. "Phylogeny, classification and diversity of Choreotrichia and Oligotrichia (Ciliophora, Spirotrichea)" . Molecular Phylogenetics and Evolution, vol. 112, 2017, pp. 12-22.
---------- VANCOUVER ----------
Santoferrara, L.F., Alder, V.V., McManus, G.B. Phylogeny, classification and diversity of Choreotrichia and Oligotrichia (Ciliophora, Spirotrichea). Mol. Phylogenet. Evol. 2017;112:12-22.