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Phylogenomic analyses support the bifurcation of ciliates into two major clades that differ in properties of nuclear division

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Highlights

  • A taxon-rich phylogenomic strategy was used to assess the evolutionary relationships within ciliates.

  • 537 taxa combined with a moderate number of proteins were accessed from GenBank and recently released transcriptome data.

  • Full data matrix as well as six submatrices were analyzed to assess the impact of taxon sampling and missing data.

  • The multigene phylogenies support the bifurcation of ciliates into two major clades as suggested by SSU-rDNA.

Abstract

Ciliates are a diverse assemblage of eukaryotes that have been the source of many discoveries including self-splicing RNAs, telomeres and trans-splicing. While analyses of ciliate morphology have given rise to robust hypotheses on relatively shallow level relationships, the deeper evolutionary history of ciliates is largely unknown. This is in part because studies to date have focused on only a single locus, small subunit ribosomal DNA (SSU-rDNA). In the present study, we use a taxon-rich strategy based on multiple loci from GenBank and recently completed transcriptomes to assess deep phylogenetic relationships among ciliates. Our phylogenomic data set includes up to 537 taxa, all of which have been sampled for SSU-rDNA and a subset of which have LSU-rDNA and up to 7 protein-coding sequences. Analyses of these data support the bifurcation of ciliates as suggested by SSU-rDNA, with one major clade defined by having somatic macronuclei that divide with intranuclear microtubules (Intramacronucleata) and the other clade containing lineages that either divide their macronuclei with microtubules external to the macronucleus or are unable to divide their macronuclei (Postciliodesmatophora). These multigene phylogenies provide a robust framework for interpreting the evolution of innovations across the ciliate tree of life.

Introduction

Ciliates are characterized by the presence of cilia in at least one of their life stages and by their nuclear dimorphism (i.e. the presence of a somatic macronucleus and a germline micronucleus in each cell). Following conjugation, macronuclei derive from zygotic nuclei through chromosomal rearrangements that include fragmentation, elimination of internal sequences and amplification of the processed chromosomes; in all but one class of ciliates (Karyorelictea, see below) the resulting macronuclei divide by amitosis during asexual division (Prescott, 1994). Given their age of approximately one billion years (Parfrey et al., 2011), estimation of deep relationships within this clade are difficult.

The class Karyorelictea Corliss, 1974 had been argued to be sister to all other ciliates based on the relatively simple morphologies and the presence of nearly-diploid, non-dividing macronuclei within this clade (Raikov, 2006). Subsequent phylogenetic analyses of ciliates based only on SSU-rDNA divides ciliates into two clades, Intramacronucleata Lynn, 1996 and Postciliodesmatophora Gerassimova and Seravin, 1976 (Lynn, 1996). The Intramacronucleata includes the bulk of the ciliate classes such as Oligohymenophorea (e.g. Paramecium and Tetrahymena), and are united by the feature of division of the macronucleus involving intramacronuclear microtubules (Hirt et al., 1995, Lukashenko, 2009, Lynn, 1996). In contrast, ciliates in Postciliodesmatophora either have macronuclei that cannot divide (i.e. Karyorelictea) or macronuclei that divide with microtubules external to the macronucleus (i.e. Heterotrichea).

Given the limitation of single gene trees, we use a taxon-rich strategy based on multiple loci to assess the relationships within ciliates. We expand the taxonomic sampling of SSU-rDNA to 537 species representing all major ciliate lineages and combine these data with large subunit-rDNA and up to seven protein genes from a subset of taxa. We analyzed the full data matrix as well as six submatrices to assess the impact of taxon sampling and missing data.

Section snippets

Dataset assembly

We collected small subunit ribosomal DNA (SSU-rDNA) and large subunit ribosomal DNA (LSU-rDNA) sequences for all the ciliates from GenBank using a custom Python script. The SSU-rDNA of Philasterides armatalis (FJ848877) and LSU-rDNA of Stylonychia lemnae (AF508773) were used as queries in a Blast analysis against the GenBank nr database and one sequence  1000 bp per taxon ID was kept. The taxon IDs of the ciliates from GenBank were downloaded in February 2012. Environmental and uncultured

Results and discussion

Overall, our phylogenomic analyses support the bifurcation of ciliates into two major clades defined by differences in division of the somatic macronuclei: Intramacronucleata and Postciliodesmatophora. Both clades are recovered in the tree reconstructed in our largest dataset, including 537 ciliates and all 9 genes (i.e. 2 rDNAs + 7 protein-coding; denoted all:9), with high support (89% BS and 100% BS respectively, Fig. 1). To test whether the topology is dependent on the nearly ubiquitous

Acknowledgments

This work is supported by an AREA award from the National Institutes of Health (1R15GM081865-01) to L.A.K. We would like to thank Ms. Jessica R. Grant for help with python script and data analyses. We also thank Dr. George B. McManus for sharing the transcriptome data, which were sequenced through the MMETSP (http://marinemicroeukaryotes.org/).

References (20)

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