Barcoding Tetrahymena: Discriminating Species and Identifying Unknowns Using the Cytochrome c Oxidase Subunit I (cox-1) Barcode

Kher, Chandni P.; Doerder, F. Paul; Cooper, Jason K.; Ikonomi, Pranvera; Achilles-Day, Undine E.M.; Küpper, Frithjof C.; Lynn, Denis H.

doi:10.1016/j.protis.2010.03.004

Cited by 64 publications

(78 citation statements)

References 31 publications

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“…The mitochondrial cox 1barcodes reported by Chantangsi et al [25] and Kher et al [33] are better able to discriminate among Tetrahymena species than nuclear SSU sequences. Using the extensive collection of Tetrahymena species in the American Type Culture Collection these authors defined a 689 nucleotide cox 1 barcode and provided ~1600–2300 SSU nucleotide sequences for most named Tetrahymena species.…”

Section: Methodsmentioning

confidence: 99%

“…Using the extensive collection of Tetrahymena species in the American Type Culture Collection these authors defined a 689 nucleotide cox 1 barcode and provided ~1600–2300 SSU nucleotide sequences for most named Tetrahymena species. Kher et al [33] also showed that unknowns can, in most instances, be identified by the cox 1 barcodes. The cox 1 sequence of the type strain (Table 1) designated by Chantangsi et al [25] and Kher et al .…”

Section: Methodsmentioning

confidence: 99%

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Abandoning sex: multiple origins of asexuality in the ciliate Tetrahymena

Doerder

2014

BMC Evol Biol

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BackgroundBy segregating somatic and germinal functions into large, compound macronuclei and small diploid micronuclei, respectively, ciliates can explore sexuality in ways other eukaryotes cannot. Sex, for instance, is not for reproduction but for nuclear replacement in the two cells temporarily joined in conjugation. With equal contributions from both conjugants, there is no cost of sex which theory predicts should favor asexuality. Yet ciliate asexuality is rare. The exceptional Tetrahymena has abandoned sex through loss of the micronucleus; its amicronucleates are abundant in nature where they reproduce by binary fission but never form conjugating pairs. A possible reason for their abundance is that the Tetrahymena macronucleus does not accumulate mutations as proposed by Muller’s ratchet. As such, Tetrahymena amicronucleates have the potential to be very old. This study used cytochrome oxidase-1 barcodes to determine the phylogenetic origin and relative age of amicronucleates isolated from nature.ResultsAmicronucleates constituted 25% of Tetrahymena-like wild isolates. Of the 244 amicronucleates examined for cox1 barcodes, 237 belonged to Tetrahymena, seven to other genera. Sixty percent originated from 12 named species or barcoded strains, including the model Tetrahymena thermophila, while the remaining 40% represent 19 putative new species, eight of which have micronucleate counterparts and 11 of which are known only as amicronucleates. In some instances, cox1 haplotypes were shared among micronucleate and amicronucleates collected from the same source. Phylogenetic analysis showed that most amicronucleates belong to the “borealis” clade in which mating type is determined by gene rearrangement. Some amicronucleate species were clustered on the SSU phylogenetic tree and had longer branch lengths, indicating more ancient origin.ConclusionsNaturally occurring Tetrahymena amicronucleates have multiple origins, arising from numerous species. Likely many more new species remain to be discovered. Shared haplotypes indicate that some are of contemporary origin, while phylogeny indicates that others may be millions of years old. The apparent success of amicronucleate Tetrahymena may be because macronuclear assortment and recombination allow them to avoid Muller’s ratchet, incorporate beneficial mutations, and evolve independently of sex. The inability of amicronucleates to mate may be the result of error(s) in mating type gene rearrangement.

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Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Abandoning sex: multiple origins of asexuality in the ciliate Tetrahymena

Doerder

2014

BMC Evol Biol

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“…This unresolved internal relationship raises the question whether these sequences are from different populations of one species. Since designations of the species in the T. pyriformis complex are based on a combination of ecological, morphological, biochemical, and molecular features, it is likely that the SSU rRNA gene is too conserved to reveal interspecific variation within the genus Tetrahymena (Kher et al 2011). The cox1 gene of two geographically isolated populations of T. australis, i.e.…”

Section: Comparison Of the Wuhan Population Of Tetrahymena Australis mentioning

confidence: 99%

Tetrahymena australis (Protozoa, Ciliophora): A Well‐Known But “Non‐Existing” Taxon – Consideration of Its Identification, Definition and Systematic Position

Liu

Fan

Gao

et al. 2016

J Eukaryotic Microbiology

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A cryptic species of the Tetrahymena pyriformis complex, Tetrahymena australis, has been known for a long time but never properly diagnosed based on taxonomic methods. The species name is thus invalid according to the International Code of Zoological Nomenclature. Recently, a population isolated from a freshwater lake in Wuhan, China was investigated using live observations, silver staining methods and gene sequence data. This organism can be separated from other described species of the T. pyriformis complex by its relatively small body size, the number of somatic kineties and differences in sequences of two genes, namely the small subunit ribosomal RNA (SSU rRNA) and the mitochondrial cytochrome c oxidase subunit I (cox1). We compared the SSU rRNA gene sequences of all available Tetrahymena species to reveal the nucleotide differences within this genus. The sequence of the Wuhan population is identical to two sequences of a previously isolated strain of T. australis (ATCC #30831). Phylogenetic analyses indicate that these three sequences (X56167, M98015, KT334373) cluster with Tetrahymena shanghaiensis (EF070256) in a polytomy. However, sequence divergence of the cox1 gene between the Wuhan population and another strain of T. australis (ATCC #30271) is 1.4%, suggesting that these may represent different subspecies.A wide variety of protists, including hymenostome ciliates, have relatively simple body structures with few morphological characters for species circumscription, which makes them difficult to separate from each other (Borden et al. 1977;Simon et al. 2008). Early taxonomists identified and classified such organisms based only on morphological and cell cycle characters. As a consequence, independent species were sometimes misidentified as morphologically similar species within a morphospecies complex (for instance, Paramecium aurelia). The development of modern methods, especially gene sequencing and phylogenetic analyses, has improved this situation and the taxonomic positions of several such species have been clarified in recent years (Quintela-Alonso et al. 2013;Zhao et al. 2016).Cryptic species of ciliates were first discovered by Sonneborn (1939) for the model organism P. aurelia Ehrenberg, 1838. Cryptic species have since been found in a variety of ciliate genera including Aspidisca, Colpidium, Euplotes, Glaucoma, Oxytricha, Paramecium, Pseudourostyla, Stylonychia, Tetrahymena, Tokophrya, and Uronychia (Dini and Nyberg 1993;Przybos 1986;Simon et al. 2008). The probable wide occurrence of cryptic speciation has been cited as evidence for the underestimation of ciliate species diversity (Foissner et al. 2007).Tetrahymena pyriformis (Ehrenberg, 1830) Lwoff, 1947 is another example now known to be a species complex (Nanney and McCoy 1976). Species of Tetrahymena were previously assigned to the genera Leucophyrs or Glaucoma until the establishment of the genus Tetrahymena by Furgason (1940). Using mating type tests, Gruchy (1955) first discovered the heterogeneity of T. pyriformis by describin...

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“…Thus, we assign this recent isolate from E. pacifica, the type host of P. oregonensis, to this species and provide a revised morphological characterization (see below) and genetically characterize the species using the SSU rDNA and cox1 gene sequences. Genetic characterization of ciliate species is becoming more common since extensive comparative molecular genetic research on the biological species of Tetrahymena (Kher et al 2011) and Paramecium (Strüder-Kypke & Lynn 2010, Przyboś et al 2013 using the mitochondrial cox1 gene has demonstrated significant interspecific variation. For example, Kher et al (2011) concluded that a > 5% difference in cox1 identifies different biological species of Tetrahymena, while Strüder-Kypke & Lynn (2010) concluded that this criterion rises to > 20% for biological species of Paramecium.…”

Section: T Spinifera (29) Hq965963mentioning

confidence: 99%

“…Genetic characterization of ciliate species is becoming more common since extensive comparative molecular genetic research on the biological species of Tetrahymena (Kher et al 2011) and Paramecium (Strüder-Kypke & Lynn 2010, Przyboś et al 2013 using the mitochondrial cox1 gene has demonstrated significant interspecific variation. For example, Kher et al (2011) concluded that a > 5% difference in cox1 identifies different biological species of Tetrahymena, while Strüder-Kypke & Lynn (2010) concluded that this criterion rises to > 20% for biological species of Paramecium. Biological species of Tetrahymena can have identical gene sequences for SSU rRNA, and so it is best to avoid this gene as a criterion for genetic species identification for taxonomic purposes (Strüder-Kypke & Lynn 2010).…”

Section: T Spinifera (29) Hq965963mentioning

confidence: 99%

Ciliate species diversity and host-parasitoid codiversification in Pseudocollinia infecting krill, with description of Pseudocollinia similis sp. nov.

Gómez‐Gutiérrez¹,

Strüder‐Kypke²,

Shaw³

2014

Dis. Aquat. Org.

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All parasitoid apostome ciliates infecting krill in the northeastern Pacific are currently assigned to the genus Pseudocollinia. Each krill specimen is apparently infected by only 1 Pseudocollinia species. We describe Pseudocollinia similis sp. nov., discovered infecting the krill Thysanoessa spinifera off Oregon, USA. Its protomite-tomite stage resembles that of P. beringensis, which infects T. inermis (type host species), T. longipes, and T. raschii females in the Bering Sea. These ciliates have similar numbers of somatic kineties (18-21 vs. 16-20) and typically have 3 oral kineties. Furthermore, these 2 apostomes are sister species on gene trees based on sequences of small subunit rRNA (0.06% difference) and cytochrome c oxidase subunit 1 (cox1; 30% difference). P. brintoni and P. oregonensis are closely related as a separate group from P. similis and P. beringensis. The similar tree topologies based on the cox1 sequences of 21 host krill individuals representing 6 krill species (Euphausia pacifica, Nyctiphanes simplex, T. inermis, T. longipes, T. raschii, and T. spinifera) and the apostomes isolated from these krill suggest host-parasitoid codiversification. However, this hypothesis was statistically rejected by an approximately unbiased test in which the host tree topology was used to model parasitoid evolution (p ≤ 0.05).

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Barcoding Tetrahymena: Discriminating Species and Identifying Unknowns Using the Cytochrome c Oxidase Subunit I (cox-1) Barcode

Cited by 64 publications

References 31 publications

Abandoning sex: multiple origins of asexuality in the ciliate Tetrahymena

Abandoning sex: multiple origins of asexuality in the ciliate Tetrahymena

Tetrahymena australis (Protozoa, Ciliophora): A Well‐Known But “Non‐Existing” Taxon – Consideration of Its Identification, Definition and Systematic Position

Ciliate species diversity and host-parasitoid codiversification in Pseudocollinia infecting krill, with description of Pseudocollinia similis sp. nov.

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