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Open Access Research article

Molecular phylogeny of diplomonads and enteromonads based on SSU rRNA, alpha-tubulin and HSP90 genes: Implications for the evolutionary history of the double karyomastigont of diplomonads

Martin Kolisko12, Ivan Cepicka3, Vladimir Hampl4, Jessica Leigh2, Andrew J Roger2, Jaroslav Kulda4, Alastair GB Simpson1* and Jaroslav Flegr4

Author Affiliations

1 Department of Biology, Dalhousie University. Life Sciences Centre, 1355 Oxford Street, Halifax, NS, B3H 4J1, Canada

2 Department of Biochemistry and Molecular Biology, Dalhousie University. Sir Charles Tupper Medical Building, 5850 College Street, Halifax, NS, B3H 1X5, Canada

3 Department of Zoology, Faculty of Science, Charles University in Prague. Vinicna 7, Prague, 128 44, Czech Republic

4 Department of Parasitology, Faculty of Science, Charles University in Prague. Vinicna 7, Prague, 128 44, Czech Republic

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BMC Evolutionary Biology 2008, 8:205  doi:10.1186/1471-2148-8-205

Published: 15 July 2008

Abstract

Background

Fornicata is a relatively recently established group of protists that includes the diplokaryotic diplomonads (which have two similar nuclei per cell), and the monokaryotic enteromonads, retortamonads and Carpediemonas, with the more typical one nucleus per cell. The monophyly of the group was confirmed by molecular phylogenetic studies, but neither the internal phylogeny nor its position on the eukaryotic tree has been clearly resolved.

Results

Here we have introduced data for three genes (SSU rRNA, α-tubulin and HSP90) with a wide taxonomic sampling of Fornicata, including ten isolates of enteromonads, representing the genera Trimitus and Enteromonas, and a new undescribed enteromonad genus. The diplomonad sequences formed two main clades in individual gene and combined gene analyses, with Giardia (and Octomitus) on one side of the basal divergence and Spironucleus, Hexamita and Trepomonas on the other. Contrary to earlier evolutionary scenarios, none of the studied enteromonads appeared basal to diplokaryotic diplomonads. Instead, the enteromonad isolates were all robustly situated within the second of the two diplomonad clades. Furthermore, our analyses suggested that enteromonads do not constitute a monophyletic group, and enteromonad monophyly was statistically rejected in 'approximately unbiased' tests of the combined gene data.

Conclusion

We suggest that all higher taxa intended to unite multiple enteromonad genera be abandoned, that Trimitus and Enteromonas be considered as part of Hexamitinae, and that the term 'enteromonads' be used in a strictly utilitarian sense. Our result suggests either that the diplokaryotic condition characteristic of diplomonads arose several times independently, or that the monokaryotic cell of enteromonads originated several times independently by secondary reduction from the diplokaryotic state. Both scenarios are evolutionarily complex. More comparative data on the similarity of the genomes of the two nuclei of diplomonads will be necessary to resolve which evolutionary scenario is more probable.